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THE LIFE OF

VERTEBRATES

THE LIFE OF

VERTEBRATES

J. Z. YOUNG

M.A., F.R.S.

PROFESSOR OF ANATOMY AT
UNIVERSITY COLLEGE, LONDON

SECOND EDITION

OXFORD UNIVERSITY PRESS

NEW YORK & OXFORD

1962

First Edition 1950
Second Edition 1962

Printed in the United States of America

ACKNOWLEDGEMENTS

My grateful thanks are due to the following, who spent much time reading and
criticizing various parts of the manuscripts and proofs:

E. H. Ashton, A. d'A. Bellairs, Q. Bone, B. B. Boycott, P. M. Butler, S. Crowell,

D. H. Cushing, F. C. Fraser, R. B. Freeman, H. Greenwood, I. Griffiths, R. J.
Harrison, R. A. Hinde, K. A. Kermack, J. Lever, N. B. Marshall, D. R. Newth,
C. Nicol, F. R. Parrington, P. Robinson, A. J. Sutcliffe, H. G. Vevers, E. I.
White, M. Whitear.

Thanks for permission for reproductions of illustrations are due to:

G. C. Aymar, E. J. W. Barrington, J. Berrill, T. H. Bullock, A. J. E. Cave,
W. E. Le Gros Clark, E. Crosby, F. G. Evans, Helen Goodrich, A. Gorbman,
J. Gray, W. K. Gregory, W. J. Hamilton, J. E. Harris, L. Hogben, A. Holmes,

E. Hoskings, W. W. Howells, J. S. Huxley, F. Knowles, D. Lack, N. A. Mackin-
tosh, G. H. Parker, A. T. Phillipson, R. J. Pumphrey, E. C. R. Reeve, A. S.
Romer, E. S. Russell, F. K. Sanders, A. H. Schultz, G. G. Simpson, N. Tinber-
gen, G. L. Walls, L. Waring, T. S. Westoll, E. I. White, F. F. Zeuner,

and to the following publishers and other bodies:

The American Museum of Natural History; Bailliere, Tindall and Cox; E.
Benn, Ltd. ; Biological Reviezvs ; the British Medical Journal; the British Museum ;
the Cambridge University Press; the Company of Biologists, Ltd.; Dodd, Mead
& Co.; Editors of the Ibis; Longmans, Green & Co., Ltd.; the Physiological
Society; Putnam, Ltd.; the Scientific Monthly; the Wilson Bulletin; the Wistar
Institute; Zoological Society of London.

PREFACE TO
THE SECOND EDITION

For this edition every part of the book has been revised and corrected,
but the basic plan and balance of interests have not been altered.
Changes of arrangement and emphasis might have suited some types
of reader but I have thought it better that the book should continue
to show the idiosyncracies and interests of the author. One of the
dangers of a textbook is, surely, that unsophisticated readers may sup-
pose that they are getting the authentic and complete treatment of the
subject. Some obvious imbalances may, therefore, even be an advan-
tage as reminders of the relativity of all statements.

Nevertheless, I have attempted to make the treatment rather more
complete and systematic than before. For example, the descriptions
of the parts of the body are now arranged more nearly similarly for all
groups. With the help of many friends mistakes have been removed
and accounts of recent work added. The anatomy of Mammals is not
dealt with in the same detail as that of other groups, being covered
separately in The Life of Mammals (Clarendon Press, 1957), where
also there is a fuller account of the comparative embryology of
vertebrates.

During the revision I have become even more conscious of the
defects of the work, both in general form and detailed treatment. It is
still not possible to see more than the vaguest outlines of a proper
science of comparative biology. We are faced with a great series of
wonderful systems, differing slightly from each other and maintaining
themselves in slightly different surroundings. But we have no proper
scientific words with which to talk about them. For example, it is
absurd that this book contains so little reference to genetics, bio-
chemistry, or control theory. No doubt this is partly my fault, but the
fact is that these more exact sciences have yet to show us how to treat
the organization of a whole creature.

Fortunately, the animals remain as fascinating as ever, indeed the
search for exact ways of describing makes them even more so. Those
of us who have revised the book will be well rewarded for our trouble
if others arc helped to look and think for themselves. If they do they
will find a really astonishing array of experiments made by natural
selection with every part of the vertebrate organization. To take one
example, we are offered the opportunity to learn how the endocrine

vi PREFACE TO SECOND EDITION

control system works by examining hundreds of different variants of
it. The more one thinks of it the more surprising it is that biology
has made so little use of the experiments that have been done for us
by nature. Surely soon someone will come along with sufficient know-
ledge and logical and mathematical ingenuity to show us how to study
vertebrate organization.

Besides those mentioned below who have assisted in the revision of
particular sections, I should like to thank the many people, including
teachers and students, who have written about particular points, and
especially Professor J. Lever of Amsterdam for his many detailed
comments. My grateful thanks are also due to Mrs. J. Astafiev, who
has redrawn many of the figures, Mr. C. Marmoy for assistance with
the Bibliography, Mr. P. N. Dilly, who has helped throughout, also
my secretaries and especially Miss S. Thistleton and Miss J. Everard,
for continuous help with the manuscript. It is also a pleasure to thank
the members of the Clarendon Press and in particular Miss M. Gregory
for the help with the revision.

J. Z. Y.

February 1962

PREFACE TO
THE FIRST EDITION

The history of textbooks is often dismissed by the contemptuous
assertion that they all copy each other — and especially each other's
mistakes. Inspection of this book will quickly confirm that this is true,
but there is nevertheless an interest to be obtained from such a study,
because textbooks embody an attitude of mind; they show what sort
of knowledge the writer thinks can be conveyed about the subject-
matter. It may be that they are more important than at first appears
in furthering or preventing the change of ideas on any theme.

The results of the studies of scholars on the subject of vertebrates
have been summarized in a series of comprehensive textbooks during
the past hundred years. Most of these works are planned on the lines
laid down by the books of Gegenbaur (1859), Owen (1866), and
Wiedersheim (1883), lines that derive from a pre-evolutionary tradi-
tion. This partly explains the curiosity that in spite of the great impor-
tance of evolutionary doctrine for vertebrate studies, and vice versa,
vertebrate textbooks often do not deal directly with evolution. They
derive their order from something even more fundamental than the
evolutionary principle. The essential of any good textbook is that it
should be both accurate and general. As Owen puts it in his Preface:
Tn the choice of facts I have been guided by their authenticity and
their applicability to general principles.' The chief of the principles
he adopted was 'to guide or help in the power of apprehending the
unity which underlies the diversity of animal structures, to show in
these structures the evidence of a predetermining Will, producing
them in reference to a final purpose, and to indicate the direction and
degrees in which organisation, in subserving such Will, rises from the
general to the particular'. He confessed 'ignorance of the mode of
operation of the natural law of their succession on the earth. But that
it is an "orderly succession" — and also "progressive" — is evident
from actual knowledge of extinct species.'

These principles were essentially sound, and Owen's treatment was
to a large extent the basis of the work that appeared after the Dar-
winian revolution. In English, following the translation of Wieder-
sheim's book by W. N. Parker (1886) we have H. J. Parker and
Haswell's work, now in its 6th edition. The books of Kingsley and
Neal and Rand are in essentially the same tradition, though they

viii PREFACE TO FIRST EDITION

incorporate much new work, especially from the neurological studies
of Johnston and Herrick. Further exact studies on these same general
morphological lines made possible the books of Goodrich (1930) and
de Beer (1935), which have provided the morphological background
for the present work. Throughout these works on Comparative Ana-
tomy the emphasis is on the evolution of the form of each organ
system rather than on the change of the organization of the life of
the animal as a whole.

Meanwhile many other treatises appeared dealing with the life and
habits of the animals, rather than with morphological principles.
Among these we may mention Bronn's Tierreich (1859 onwards), the
Cambridge Natural History, and many works dealing with particular
groups of vertebrates. The palaeontologists produced their own series
of textbooks, mainly descriptive, such as those of Zittel and Smith
Woodward, culminating in Romer's admirably detailed and concise
book, to which the present work owes very much. The results of
embryological work have been summarized by Graham Kerr (191 9),
Korscheldt and Heider (1931), Brachet (1935), Huxley and de Beer
(1934), and Weiss (1939), among others. Unfortunately there has been
little summarizing of what is commonly called the comparative physio-
logy of vertebrates. Winterstein's great Handbuch der vergleichenden
Physiologie (191 2) covers much detailed evidence, but comes no nearer
than do the comparative anatomists to giving us a picture of the
evolution of the life of the whole organism.

All of these books deal in some way with the evolution of vertebrates,
and vet curiously enough they speak of it very little. It is hardly an
exaggeration to say that they leave the student to decide for himself
what has been demonstrated by their studies. Huxley's Anatomy of
Vertebrated Animals (1871) is an exception in that it deals with the
animals rather than their parts, and at a more popular level. Brehm's
Thierleben (1876) gives a picture of the life of the animals, though in
this case not of their underlying organization. Kukenthal's great
Handbuch der Zoologie has the aim of synthesizing a variety of know-
ledge about each animal-group, and some of the volumes dealing with
vertebrates make fascinating reading- — notably that of Streseman on
birds. But the size of the work and the multiplicity of authors make
it impossible for any general picture of vertebrate life to appear from
the mass of details.

The position is, then, that we have good descriptions of the struc-
ture, physiology, and development of vertebrates, of the discoveries
of the palaeontologists and accounts of vertebrate natural history, but

PREFACE TO FIRST EDITION ix

that there is no work that attempts to define the organization of the
whole life and its evolution in all its aspects. Indeed, none of these
works defines what is being studied or tries to alter the direction of
investigation — all authors seem prepared to agree that biological study
is adequately expressed through the familiar disciplines of anatomy,
physiology, palaeontology, embryology, or natural history. In passing,
we may note the extraordinary fact that there are no detailed works on
the comparative histology or biochemistry of vertebrates — surely most
fascinating fields for the future, as is, indeed, hinted by the attempts
that have been made in older works, such as that of Ranvier (1878),
and the newer ones of Baldwin (1937 and 1945).

The present book has gradually grown into an attempt to define
what is meant by the life of vertebrates and by the evolution of that
life. Put in a more old-fashioned way, this represents an attempt to
give a combined account of the embryology, anatomy, physiology,
biochemistry, palaeontology, and ecology of all vertebrates. One of
the results of the work has been to convince me more than ever that
these divisions are not acceptable. All of their separate studies are
concerned with the central fact of biology, that life goes on, and I
have tried to combine their results into a single work on the way in
which this continuity is maintained.

A glance through the book will show that I have not been successful
in producing anything very novel — others will certainly be able to
go much farther, and in particular to introduce to a greater extent facts
about the evolution of the chemical and energy interchanges of verte-
brates, here almost omitted! However, I have very much enjoyed the
attempt, which has provided the stimulus to try to find out many
things that I have always wanted to know.

For any one person to cover such a wide field is bound to lead to
inexactness and error in many places. I have tried to verify from
nature as often as possible, but a large amount has been copied, no
doubt often wrongly. Throughout, the aim has been to provide
wherever possible an idea of the actual observations that have been
made, as well as the interpretations placed upon them. A proper
appraisal of general theories can only be reached if there is first a
knowledge of the actual materials, which is the characteristic feature
of scientific observation. A book such as the present has value only
in so far as it leads the reader to make his own observations and helps
him to know the world for himself.

Mammalian organization requires more detailed treatment than
that of other groups, and in providing this the work grew to beyond

x PREFACE TO FIRST EDITION

the length of a single book. Mammalian structure, function, and
development will therefore be dealt with in a separate volume, which
will also include a survey of comparative embryology.

The original plan was that the palaeontological parts of the book
would be written by J. A. Moy-Thomas. Had he lived this aspect of
the work would have been very much better, and his common sense
and laughter would have lightened the whole. I have tried to give
some compensation at least by the speculation that is possible from a
single point of view. To protect the reader against the limitations of
my ignorance I have consulted specialists on every part of the work,
and my deepest thanks are due to those who have helped in this way.
They have done wonders in correcting mistakes, but, of course, are
not responsible for any that remain, or for views expressed. Among
those who have helped in this way with particular parts are Professor
G. R. de Beer, Mr. R. B. Freeman, the late Professor W. Garstang,
Dr. A. Graham, Professor J. B. S. Haldane, Professor W. Holling-
worth, Dr. W. Holmes, Dr. J. S. Huxley, Dr. D. Lack, Mr. Maynard
Smith, Dr. F. S. Russell, Dr. Tyndell Hopwood, Mr. H. G. Vevers,
Professor D. M. S. Watson, and Professor S. Westoll. They have been
patient and severe critics, and the reader and I owe them very much.

One of the main problems of such a work is its illustration, and here
I have been extraordinarily fortunate in having the help of Miss E. R.
Turlington, who has not only provided brilliantly clear and beautiful
pictures, but has taken extremes of care to ensure their accuracy by
drawing from live animals, from dissections, and from skeletons, as
well as by research into the illustrations of others. Miss J. de Vere
has also given much help with drawing. We have borrowed good
pictures unhesitatingly and should like to thank those who have given
permission for their reproduction.

I should also like to thank particularly my secretary, Miss P. Codlin,
who has played a large part in making the book possible, and my
daughter Cordelia for help with the index.

Finally, I have to thank the Secretary and members of Oxford
University Press for the care with which the book has been produced,
and for their friendly co-operation, which has made the work a
pleasure.

J. Z. Y.

1950

CONTENTS

I. EVOLUTION OF LIFE IN RELATION TO CLIMATIC AND GEO-

LOGICAL CHANGE

i. The need for generality in zoology, i ; 2. What do we mean by the life of an
animal ? 2; 3. Li ving things tend to preserve themselves, 3; 4. What do we mean by
awareness of life ? 5 ; 5. The influence of environment on life, 7 ; 6. What is it that
heredity transmits ? 8 ; 7. The increasing complexity of life, 9 ; 8. The progression
of life from the water to more difficult environments, 9; 9. Changes of climate and
geological periods — (1) Changes of level of the continents, 11; (2) Changes of
climate, 13; (3) Geological time, 16; (4) Classification of geological history, 18;
10. Summary, 21.

II. THE GENERAL PLAN OF CHORDATE ORGANIZATION: AMPHI-

OXUS

1. The variety of chordate life, 23; 2. Classification of chordates, 24; 3. Amphi-
oxus, a generalized chordate, 24; 4. Movement of amphioxus, 26; 5. Skeletal
structures of amphioxus, 29; 6. Skin of amphioxus, 29; 7. Mouth and pharynx
and the control of feeding, 30; 8. Circulation, 33; 9. Excretory system of
amphioxus, 35; 10. Nervous system, 36; 11. Gonads and development of
amphioxus, 41; 12. Amphioxus as a generalized chordate, 46.

III. THE ORIGIN OF CHORDATES FROM FILTER FEEDING ANIMALS
1. Invertebrate relatives of the chordates, 47; 2. Subphylum Hemichordata
(= Stomochordata), 50; 3. Class Pterobranchia, 58; 4. Subphylum Tunicata.
Sea squirts, 60; 5. Development of ascidians, 66; 6. Various forms of tunicate,
69; 7. Class Ascidiacea. 70; 8. Class Thaliacea, 70; 9. Class Larvacea, 72;

10. The formation of the chordates, 74.

IV. THE VERTEBRATES WITHOUT JAWS. LAMPREYS

1. Classification, 81; 2. General features of vertebrates, 81; 3. Agnatha, 83;
4. Lampreys, 83; 5. Skeleton of lampreys, 85; 6. Alimentary canal of lampreys,
88; 7. Blood system of lampreys, 91; 8. Urinogenital system of lampreys, 93;
9. Nervous system of lampreys, 97; 10. The pineal eyes, 103; 1 1. Pituitary body
and hypophyseal sac, 106; 12. Lateral line organs of lampreys, 108; 13. Vesti-
bular organs of lampreys, 109; 14. Paired eyes of lampreys, no; 15. Skin photo-
receptors, in; 16. Habits and life-history of lampreys, 112; 17. The ammocoete
larva, 114; 18 Races of lampreys, a problem in systematics, 119; 19. Hag-fishes,
order Myxinoidea, 122; 20. Fossil Agnatha, the earliest-known vertebrates, 125.

V. THE APPEARANCE OF JAWS. THE ORGANIZATION OF THE HEAD
1. The elasmobranchs : introduction, 131; 2. The swimming of fishes, 133;
3. Equilibrium of fishes in water; the functions of the fins, 136; 4. Skin of
elasmobranchs, 141; 5. The skull and branchial arches, 142; 6. The jaws, 145;
7. Segmentation of the vertebrate head, 148; 8. The pro-otic somites and eye-
muscles, 149; 9. The cranial nerves of elasmobranchs, 152; 10. Respiration, 157;

11. The gut of elasmobranchs, 158; 12. The circulatory system, 159; 13. Urino-
genital system, 162; 14. Endocrine glands of elasmobranchs, 164; 15. Nervous
system, 167; 16. Receptor-organs of elasmobranchs, 170; 17. Autonomic nervous
system, 173.

81659

xii CONTENTS

VI. EVOLUTION AND ADAPTIVE RADIATION OF ELASMOBRANCHS
i. Characteristics of elasmobranchs, 175; 2. Classification, 175; 3. Palaeozoic
elasmobranchs, 176; 4. Mesozoic sharks, 180; 5. Modern sharks, 180; 6. Skates
and rays, 182; 7. Chimaera and the bradyodonts, 184; 8. Tendencies in elasmo-
branch evolution, 185; 9. The earliest Gnathostomes, Placoderms, 186.

VII. THE MASTERY OF THE WATER. BONY FISHES

1. Introduction: the success of the bony fishes, 190; 2. The trout, 191; 3. The
skull of bony fishes, 193; 4. Respiration, 196; 5. Vertebral column and fins
of bony fishes, 199; 6. Alimentary canal, 201 ; 7. Air-bladder, 201 ; 8. Circulatory
system, 201 ; 9. Urinogenital system and osmoregulation, 202; 10. Races of trout
and salmon and their breeding habits, 204; 1 1. Endocrine glands of bony fishes,
206; 12. Brain of bony fishes, 209; 13. Receptors for life in the water, 212;
14. Eyes, 212; 15. Ear and hearing of fishes, 216; 16. Sound production in
fishes, 218; 17. The lateral line organs of fishes, 218; 18. Chemoreceptors.
Taste and smell, 220; 19. Touch, 222; 20. Autonomic nervous system, 222;
21. Behaviour patterns of fishes, 225.

VIII. THE EVOLUTION OF BONY FISHES

1. Classification, 228; 2. Order 1. Palaeoniscoidei, 228; 3. Order 2. Acipen-
seroidei, 234; 4. Superorder 2. Holostei, 234; 5. Superorder 3. Teleostei, 236;

6. Analysis of evolution of the Actinopterygii, 237.

IX. THE ADAPTIVE RADIATION OF BONY FISHES

I. Swimming and locomotion, 244; 2. Various body forms and swimming habits
in teleosts, 248; 3. Structure of mouth and feeding-habits of bony fishes, 251;
4. Protective mechanisms of bony fishes, 252; 5. Scales and other surface armour,
252; 6. Spines and poison glands, 253; 7. Electric organs, 253; 8. Luminous
organs, 254; 9. Colours of fishes, 255; 10. Colour change in teleosts, 258;

II. Aerial respiration and the air-bladder, 261; 12. Special reproductive
mechanisms in teleosts, 265.

X. LUNG-FISHES

1. Classification, 268; 2. Crossopterygians, 268; 3. Osteolepids, 268; 4. Coela-
canths, 271; 5. Fossil Dipnoi, 273; 6. Modern lung-fishes, 275.

XI. FISHES AND MAN, 280

XII. TERRESTRIAL VERTEBRATES: AMPHIBIA

1. Classification, 296; 2. Amphibia, 296; 3. The frogs, 298; 4. Skin of Amphibia,
298; 5. Colours of Amphibia, 299; 6. Vertebral column of Amphibia, 303;

7. Evolution and plan of the limbs of Amphibia, 307; 8. Shoulder girdle of
Amphibia, 309; 9. Pelvic girdle of Amphibia, 312; 10. The limbs of Amphibia,
313; 1 1. The back and belly muscles of Amphibia, 318; 12. The limb muscles of
Amphibia, 322; 13. The skull of Stegocephalia, 325; 14. The skull of modern
Amphibia, 328; 15. Respiration in Amphibia, 332; 16. Respiration in the frog,
333; I 7- Respiratory adaptations in various amphibians, 334; 18. Vocal appara-
tus, 334; 19. Circulatory system of Amphibia, 335; 20. Lymphatic system of
Amphibia, 338; 21. The blood of Amphibia, 339; 22. Urinogenital system of
Amphibia, 340; 23. Digestive system of Amphibia, 342; 24. Nervous system
of Amphibia, 344; 25. Skin receptors, 349; 26. The eyes of Amphibia, 350; 27.
The ear of Amphibia, 353; 28. Behaviour of Amphibia, 354.

CONTENTS xiii

XIII. EVOLUTION AND ADAPTIVE RADIATION OF AMPHIBIA

i. The earliest Amphibia, 356; 2. Terrestrial Palaeozoic Amphibia. Embolomeri
and Rhachitomi, 357; 3. Aquatic Amphibia of the later Palaeozoic, 359;
4. Tendencies in the evolution of fossil Amphibia, 362; 5. Newts and Salaman-
ders. Subclass Urodela, 364; 6. Frogs and Toads. Subclass Anura, 365; 7. Sub-
class Apoda (— Gymnophiona = Caecilia), 366; 8. Adaptive radiation and
parallel evolution in modern Amphibia, 366; 9. Can Amphibia be said to be
higher animals than fishes ? 367.

XIV. LIFE ON LAND: THE REPTILES

1. Classification, 369; 2. Reptilia, 371; 3. The organization of reptiles, 372;
4. Skin of reptiles, 373; 5. Posture, locomotion, and skeleton, 373; 6. Feeding
and digestion, 378; 7. Respiration, circulation, and excretion, 378; 8. Reproduc-
tion of reptiles, 380; 9. Nervous system and receptors of reptiles, 383.

XV. EVOLUTION OF THE REPTILES

1. The earliest reptile populations, Anapsida, 386; 2. Classification of reptiles,
391; 3. Order 1. Chelonia, 392; 4. Subclass *Synaptosauria, 399; 5. Order
*Ichthyopterygia, 401 ; 6. Subclass Lepidosauria, 401 ; 7. Order Rhynchocephalia,
402; 8. Order Squamata, 404; 9. Suborder Lacertilia, 407; 10. Suborder
Ophidia, 411; 11. Superorder Archosauria, 416; 12. Order *Pseudosuchia, 417;
13. Order *Phytosauria, 417; 14. Order Crocodilia, 418; 15. The 'Terrible
Lizards', Dinosaurs, 421; 16. Order *Saurischia, 422; 17. Order *Ornithischia,
424; 18. Order *Pterosauria, 426; 19. Conclusions from study of evolution of the
reptiles, 429.

XVI. LIFE IN THE AIR: THE BIRDS

1. Features of bird life, 431 ; 2. Bird numbers and variety, 431 ; 3. The skin and
feathers, 432; 4. Colours of birds, 436; 5. The skeleton of the bird. Sacral and
sternal girders, 437; 6. The sacral girder and legs, 440; 7. Skeleton of the wings,
447; 8. Wing muscles, 449; 9. Principles of bird flight, 450; 10. Wing shape,
452; 1 1. Wing area and loading, 452; 12. Aspect ratio, 453; 13. Wing tips, slots,
and camber, 453; 14. Flapping flight, 455; 15. Soaring flight, 458; 16. Soaring
on up-currents, 458; 17. Use of vertical wind variations, 460; 18. Speed of
flight, 461; 19. Take-off and landing, 462; 20. The skull in birds, 464; 21. The
jaws, beak, and feeding mechanisms, 464; 22. Digestive system of birds, 468;
23. Circulatory system, 470; 24. Respiration, 471; 25. Excretory system, 474;
26. Reproductive system, 475; 27. The brain of birds, 477; 28. Functioning of the
brain in birds, 479; 29. The eyes of birds, 482; 30. The ear of birds, 488; 31.
Other receptors, 490.

XVII. BIRD BEHAVIOUR

I. Habitat selection, 491; 2. Food selection, 491; 3. Recognition and social
behaviour, 492; 4. Bird migration and homing, 493; 5. The stimulus to migra-
tion, 495; 6. The breeding-habits of birds, 496; 7. Courtship and display, 497;
8. Bird territory, 503; 9. Mutual courtship, 504; 10. Nest-building, 505;

I I. Shape and colour of the eggs, 507; 12. Brooding and care of the young, 507.

XVIII. THE ORIGIN AND EVOLUTION OF BIRDS

1. Classification, 509; 2. Origin of the birds, 510; 3. Jurassic birds and the
origin of flight, 510; 4. Cretaceous birds. Superorder Odontognathae, 513;

xiv CONTENTS

5. Flightless birds. Superorder Palaeognathae, 514; 6. Penguins. Superorder
Impennae, 515; 7. Modern birds. Superorder Neognathae, 516; 8. Tendencies
in the evolution of birds, 522 ; 9. Darwin's finches, 524 ; 1 o. Birds on other oceanic
islands, 530; 11. The development of variety of bird life, 532.

XIX. THE ORIGIN OF MAMMALS

1. Classification, 533; 2. The characteristics of mammals, 534; 3. Mammals of
the Mesozoic, 536; 4. Mammal-like reptiles, Synapsida, 539; 5. Order *Pely-
cosauria (= Theromorpha), 540; 6. Order *Therapsida, 541; 7. Mammals from
the Trias to the Cretaceous, 545; 8. Original cusp-pattern of teeth of mammals,
548; 9. Egg-laying mammals. Subclass Prototheria (Monotremata), 549.

XX. MARSUPIALS

1. Marsupial characteristics, 557; 2. Classification of marsupials, 562; 3. Opos-
sums, 563; 4. Carnivorous marsupials, 565; 5. Marsupial ant-eaters and other
types, 566; 6. Phalangers, wallabies, and kangaroos, 566; 7. Significance of
marsupial isolation, 568.

XXI. EVOLUTION OF PLACENTAL MAMMALS AND ITS RELATION
TO THE CLIMATIC AND GEOGRAPHICAL HISTORY OF THE
CENOZOIC

1. Eutherians at the end of the Mesozoic, 569; 2. The end of the Mesozoic, 569;
3. Divisions and climates of the Tertiary Period, 571; 4. Geographical regions,
572; 5. The earliest eutherians, 574; 6. Definition of a eutherian (placental) mam-
mal) 575; 7- Evolutionary trends of eutherians, 575; 8. Conservative eutherians,
577; 9. Divisions and classification of Eutheria, 577.

XXII. INSECTIVORES, BATS, AND EDENTATES

1. Order 1. Insectivora, 581; 2. Order Chiroptera. Bats, 585; 3. Order Dermo-
ptera, 592; 4. Order Edentata, 592; 5. Armadillos, 595; 6. Ant-eaters and sloths,
597; 7. Order Pholidota: pangolins, 601.

XXIII. PRIMATES

1. Classification, 602; 2. Characters of primates, 603; 3. Divisions of the pri-
mates, 607; 4. Lemurs and lorises, 609; 5. Fossil Prosimians, 613; 6. Tarsiers,
614; 7. Characteristics of Anthropoidea, 617; 8. New World monkeys, Ceboidea,
620.

XXIV. MONKEYS, APES, AND MEN

1. Common origin of Old World monkeys, apes, and men, 623; 2. Old World
monkeys, Cercopithecoidea, 623; 3. The great apes: Pongidae, 626; 4. The
ancestry of man, 633; 5. Brain of apes and man, 633; 6. The posture and gait of
man, 634; 7. The limbs of man, 635; 8. The skull and jaws of man, 637; 9. Rate
of development of man, 640 ; 10. Growth of human populations, 641 ; 1 1 . Time of
development of the Hominidae, 641; 12. The Australopithecinae, 643; 13. Early
Hominids, *Pithecanthropus, 645; 14. Man, 646; 15. Human cultures, 648.

XXV. RODENTS AND RABBITS

1. Characteristics of rodent life, 652; 2. Classification, 653; 3. Order Rodentia,
654; 4. Order Lagomorpha, 660; 5. Fluctuations in numbers of mammals, 663.

CONTENTS xv

XXVI. WHALES, 666.

XXVII. CARNIVORES

i. Affinities of carnivores and ungulates: Cohort Ferungulata, 677; 2. Classifica-
tion, 679; 3. Order Carnivora, 680; 4. The Cats, 680; 5. *Suborder Creodonta,
683; 6. Suborder Fissipeda, 684; 7. Suborder Pinnepedia, 691.

XXVIII. PROTOUNGULATES

1. Origin of the ungulates, 694; 2. Ungulate characters, 695; 3. Classification, 699;

4. Superorder Protoungulata, 700; 5. South American ungulates. *Order Notoun-
gulata, 701; 6. *Order Litopterna, 703; 7. *Order Astrapotheria, 703; 8. Order
Tubulidentata, 704.

XXIX. ELEPHANTS AND RELATED FORMS

1. 'Near-ungulates', superorder Paenungulata, 706; 2. Classification, 706;
3. Order Hyracoidea, 707; 4. Elephants. Order Proboscidea, 709; 5. *Order
Pantodonta (Amblypoda), 717; 6. *Order Dinocerata, 718; 7. *Order Pyro-
theria, 718; 8. *Order Embrithopoda, 718; 9. Order Sirenia, 720.

XXX. PERISSODACTYLS

1. Perissodactyl characteristics, 722; 2. Classification, 723; 3. Perissodactyl
radiation, 724; 4. Suborder Ceratomorpha, tapirs and rhinoceroses, 727;

5. Rhinoceroses, 728; 6. *Brontotheres (*Titanotheres), 730; 7. *Chalicotheres
(= *Ancylopoda), 731; 8. Palaeotheres, 732; 9. Horses, 732; 10. Allometry in
the evolution of horses, 737; 11. Rate of evolution of horses, 738; 12. Conclu-
sions from the study of the evolution of horses, 739.

XXXI. ARTIODACTYLS

1. Characteristics of artiodactyls, 741; 2. Classification, 745; 3. The evolution
of artiodactyls, 746; 4. Pigs and hippopotamuses, 748; 5. *Oreodonts, 750;

6. Camels, 751; 7. Ruminants, 753; 8. Chevrotains, 754; 9. Pecora, 755;
10. Cervidae, 755; II. Giraffidae, 757; 12. Antilocapridae and Bovidae, 760.

XXXII. CONCLUSION. EVOLUTIONARY CHANGES OF THE LIFE OF
VERTEBRATES

1. The life of the earliest chordates, 765; 2. Comparison of the life of early
chordates with that of mammals, 767; 3. The increasing complexity and variety
of vertebrates, 768; 4. The variety of evidence of evolutionary change, 769;
5. Rate of evolutionary change, 770; 6. Vertebrates that have evolved slowly,
771; 7. Varying rates of evolutionary changes, 774; 8. Vertebrates that have
disappeared, 774; 9. Successive replacement among aquatic vertebrates, 775;
10. Successive replacement among land vertebrates, 776; 11. Is successive re-
placement due to climatic change?, 776; 12. Convergent and parallel evolution,
777'. ! 3- Some tendencies in vertebrate evolution, 779; 14. Evolution of the
whole organization, 780; 15. Summary of evidence about evolution of verte-
brates, 781; 16. Conservative and radical influences in evolution, 783; 17. The
direction of evolutionary change, 784; 18. The influences controlling evolutionary
progress, 785.

REFERENCES 787

INDEX 797

THE LIFE OF

VERTEBRATES

EVOLUTION OF LIFE IN RELATION TO CLIMATIC
AND GEOLOGICAL CHANGE

1 . The need for generality in zoology

The aim of any zoological study is to know about the life of the ani-
mals concerned. Our object in this book is, therefore, to help the
reader to learn as much as possible about all the vertebrate animal life
that has ever been. Thinking of the great numbers of types that have
existed since the first fishes swam in the Palaeozoic seas, one might
well be appalled by such a task: to describe all these populations in
detail would indeed demand a huge treatise. However, in a well-
developed science it should be possible to reduce the varied subject-
matter to order, to show that all differences can be understood to have
arisen by the influence of specified factors operating to modify an
original scheme. Animal and plant life is so varied that it has not yet
proved possible to systematize our knowledge of it as thoroughly as
we should wish. Thinking, again, of the variety of vertebrate lives,
it may seem impossible to imagine any general scheme and simple set
of factors that would include so many special circumstances. Yet
nothing less should be the aim of a true science of zoology. Too often
in the past we have been content to accumulate unrelated facts. It is
splendid to be aware of many details, but only by the synthesis of
these can we obtain either adequate means for handling so many
data or knowledge of the natures we are studying. In order to know
life — what it is, what it has been, and what it will be — we must
look beyond the details of individual lives and try to find rules govern-
ing all. Perhaps we may find the task less difficult than expected.
Even an elementary anatomical and physiological study shows that
all vertebrates are built upon a common plan and have certain simi-
larities of behaviour. Our object will be to come to know the nature
of this plan of life, of structure, and action, to show how it is modified
in special cases and how each special case is also an example of a
general type of modification.

Since the problem arises from the variety of animals that have
lived and live today, our central task is obviously to inquire into the
reason for the existence of so much difference. If vertebrate life began
as one single fish-like type, why has it not continued as such until
now? Why, instead of numerous identical fishes, are there countless

2 EVOLUTION OF LIFE i. i-

different kinds, while descendants of most unfish-like form are found
living out of the water and even in the air and under the ground ?

To put it in a way more familiar, though perhaps less clear: what
are the forces that have produced the changes of animal form ? Know-
ing these forces, and the original type, it would be possible to con-
struct a truly general science of zoology, with sure premisses and
deductions. Even if we cannot reach this end, we should at least try,
hoping that after investigation of the biology of vertebrates it will be
possible to retain something more than a mass of detailed information.
At the end of such a study, if we deal with the subject right, we should
surely be better able to answer some of the fundamental biological
questions. We should be able to say something about the nature of
evolution and of the differences between types, to know whether there
have been rhythms of change at work to produce these differences,
and also — the acid test of any true science — to forecast how these
changes are likely to proceed in the future.

2. What do we mean by the life of an animal?

In biology we make much use of analogies, attempting to grasp the
nature of the processes at work by comparison with man-made
machines. We have a science of anatomy, which we are told is con-
cerned with the 'structure' of animals, and we feel that we understand
what 'structure' means. Physiology is the study of 'function', and
this, too, we seem to understand. We take the analogies from our
machines, which have what we call 'structure' and 'function'. How-
ever, the difficulty at once arises that the living things make and control
themselves. The whole scheme fails us when we ask what is it, then,
that we call the 'life' of the animal, and what is it that is passed on
from generation to generation, and that changes through the ages by
the process we call evolution ? It has gradually become apparent that
the body is not a fixed, definite 'structure' as it appears to casual
observation or when dissected. In life there is ceaseless activity and
change going on within the apparently constant framework of the body.
The movement of the blood is one sign of this activity, and since
Harvey's discovery of the circulation ( 1 628) we have learnt of innumer-
able others. Everyone knows that the skin is continually being renewed
by growth from below, and many other types of cell are similarly
replaced; for instance, red blood-cells last only for a few weeks in
man. Even in the cells that are not completely destroyed and replaced,
such as the nerve-cells, there is continual change of the molecules that
make up their substance. The full extent of this exchange has been

i. 3 DEFINITION OF LIFE 3

shown by using isotopes to discover for how long individual atoms
remain in the body; the work of Schoenheimer (1942), which by this
means first clearly established the rapidity of the turnover, is a classic
of modern biology.

There are no man-made machines that replace themselves in this
way, but in recent years there has been much study of machines that
control their own operations. Such work provides us with new analo-
gies and new mathematical techniques with which we can analyse
the control of living systems (see Yockey and Quastler, 1958). As yet
we have no means of grasping the enormously complicated network
of activities that constitutes a single life. Throughout this book, how-
ever, an attempt will be made to approach that end by use of certain
clues to help us to concentrate on significant features, to see the
rhythms or patterns common to the lives of the animals, and thus to
carry in mind many details. It is possible in this way to bring together
information collected by morphologists, geneticists, embryologists,
physiologists, biophysicists, and biochemists to give a single view of
the life of the organisms concerned. The task is admittedly a hard one
and the success achieved only partial. Continually one slips into the
discussion of particular structures, substances, or processes, forgetting
the whole life. A detail of form or of chemical composition attracts,
and thus distracts, attention; perhaps it can hardly be otherwise if we
are to describe exactly. But it is surprising how practice improves the
powers of selecting and emphasizing those patterns or details of
knowledge that are significant for the study of each life as a whole.

The first difficulty is to force oneself to remember all the time that
a living animal or plant system is in a continual state of change. When
making any observations, whether by dissection or with the micro-
scope, with a test-tube, microelectrode, or respirometer, it is necessary
continually to think back to the time when the tissue was active in the
living body, and to frame the observation so that it shall reveal some-
thing significant of that activity. This means that every biologist
must know as much as possible of the life of the whole organism with
which he deals ; indeed, something of the whole population from which
the specimen was drawn.

3. Living things tend to preserve themselves

The clue by which we recognize significant features during any
biological study is that living activity tends to ensure the continuance
of its own pattern. The processes of life draw materials into the
system, organize them there, and then send them out again, all in such

4 EVOLUTION OF LIFE 1.3-

a way that the arrangement or pattern of the processes remains almost
unchanged as the molecules pass through it. We see analogies in the
way that a waterfall or a human institution such as the Catholic
Church remains the same, though its components change. Our
business is to try to describe this arrangement or pattern of processes
that is preserved. It is this pattern that we call the life of the species.
The activities that go to make up one sort of life are not necessarily
all to be found in any one individual, still less in any part of an in-
dividual. The pattern is not to be seen in any single creature or
part. Though we speak of 'individuals' they are no more the final
units than are the cells, the heart, or the brain, the bones, hair, or
nails. A whole interbreeding population is the unit of life that tends
to preserve the type, assisted, in social species, by individuals that
play a part in the life without participation in reproduction, such as
worker-bees.

A wide range of activities, therefore, goes to make up any one type
of life, and we shall only appreciate these activities properly if we study
that whole life as it is normally lived in its proper environment. The
way to study animals or men is, first and foremost, to examine them
whole, to see how their actions serve to meet the conditions of the
environment and to allow preservation of the life of the individual and
the race. Then, with this knowledge of how the animal 'uses' its parts
we may be able to make more detailed studies, down to the molecular
level, and show how together the activities form a single scheme of
action.

A living animal is continually doing things. Even when it is asleep
it is breathing, its heart beating and brain pulsing, while countless
chemical changes go on throughout its tissues. The waking life, of
course, shows this restless action even more clearly. Animals may
indeed sometimes be still, but they are never wholly inactive. It is not
difficult to see startling glimpses of this activity if we watch animals
alive, especially when they are in groups. A hawk wheeling, a pond
full of tadpoles, or a crowd of people moving on a city street will
remind us that if we are to see the interesting side of life we have to
study activity and not, as is more easy to do and so often done, to
spend all our time examining the 'structure' or 'chemistry' of the dead.

The peculiarity of this activity of animals is that much, perhaps
most, of it has the effect of maintaining the integrity of the body and,
indeed, even of increasing the bulk, or of reproducing more bodies
like the first (homeostasis). The search for food provides raw materials
giving to the muscles energy for further search. If the situation

i. 4 ACTIVITIES OF LIVING THINGS 5

demands still greater efforts these efforts will themselves lead to
'hypertrophy', or increase in the muscle substance and power. Simi-
larly, the muscular movements of respiration provide the oxygen by
which these same movements and others are made possible.

We could go on indefinitely describing how the activity of each part
of the body tends, with some exceptions, to ensure the continuation
of the whole. The mere statement of the existence of this tendency to
self-maintenance does not, perhaps, sufficiently emphasize the power
that it represents. It is one of the great 'forces' that control the
matter of the earth. It causes huge masses of material to be moved
annually to the tops of high trees and millions of wonderfully built
animals to roam daily to find and consume uncounted tons of food
or, not finding it, to search on and maintain their activity while any
calorie remains available. The power of life is sufficient to bring about
the incorporation of an appreciable part of the matter of the earth's
surface into living things. Within the appropriate range of conditions,
found chiefly near the surface of the sea and on the damper parts of
the earth, life dominates the lifeless and provides a main influence on
the matter present.

Animals and plants are able to take these actions that tend to their
own preservation because they contain stores of information about
the conditions that are likely to be met with and the means by which
adverse changes may be prevented. A fish is born with a body so
shaped that it may swim, a gull can soar on air currents, and a monkey
leap from branch to branch. Every type may thus be said to represent
the environment in which it lives, that is to say, it has a hereditary
store of information about it. Moreover, this hereditary store provides
it with receptor organs and brain with which it can acquire further
information during its lifetime. The study by engineers of the means
by which information may be coded, transmitted, and stored has
provided biologists with further means for study of the living memory
stores, which are comparable in some ways with those of machines.

4. What do we mean by awareness of life ?

A man states that he is aware that he is alive. He says that he knows
his needs and that he feels satisfaction when they are fulfilled. One
of the most difficult problems of biology is to decide how to relate
such statements about 'subjective experience' to what may be called
the 'objective' descriptions of science. This is clearly a philosophical
problem too large and important to be discussed properly here but
it must be approached. Perhaps it begins to find a solution when we

6 EVOLUTION OF LIFE 1.4-

remember that in speaking of all these matters we are using the words
of a conventional code, trying with them to convey information to
our fellows or somehow to influence them. Then we shall stop
asking such questions as 'what is consciousness ?' substituting 'what
sort of information does he transmit when he says "I am conscious" ?'

This will help with the particular aspect of the problem that con-
cerns us here. In trying to define what we mean by the 'life' of an
animal should we assume that, in addition to the actions of its body,
which we describe, there are also actions of some other entity, its
'mind' ? It is true that we should feel that any description of our own
lives that left out 'awareness' was ludicrously incomplete. Since we
have evolved from animals, so the argument runs, why should we
deny that they have some form of 'consciousness' ? This seems logical
but overlooks that the essential feature of statements such as T am
aware that I am alive' or T feel pain' is that they are part of the
means by which man, the communicating animal, controls and
influences his environment. Statements are part of human life, just
as swinging from branches is a feature of the life of monkeys and
flying of birds. It will at once be objected that these animals also
communicate, but the point is that communication must be considered
as a part of the life system of each animal, like respiration, locomotion,
or reproduction.

This leaves us with the baffling problem of finding words with
which to describe the describing system itself. Where indeed can we
find a sure basis from which to start? Here, I think, we can only
proceed by humbly admitting both ignorance and inadequacy. In
our language we have a communication system with which we can
convey to each other incomparably more information than passes
between other animals. Our system is improving every year, but it is
still grossly inadequate to describe the more subtle features of the
world, and especially of living things. We may show the greatest
respect for the depth of these mysteries by recognizing that they are
still too great for us to describe in our simple language. To provide a
good description of all the marvellous features of the life of a man or
an animal requires a complicated and subtle terminology, for which
we are striving. In pre-scientific language all such problems are
simplified by supposing that the actions of any system are produced
by some agent rather like a human being that resides within it. Thus
a child says that the clouds move 'because they want to'. So we are
accustomed to say that the body moves because it is guided by 'the
mind'. This may indeed be the best way of speaking for some

i. 5 INFLUENCE OF ENVIRONMENT 7

occasions, with our imperfect language, but it is a feeble descriptive
technique. I do not believe that it is satisfactory for biology and
especially not for zoology. By the life of an animal we mean all those
activities that make a certain pattern and serve to maintain that
pattern. In so far as we can describe this as a whole it is by comparing
it with other self-maintaining systems and particularly with those
self-controlling machines that we have made for ourselves. Biology
today has a great opportunity to explore the means by which animals
remain alive, using many sorts of descriptive technique, chemical,
electrical and, not least, the means by which mathematicians and
engineers describe whole complicated self-maintaining systems. It
is in such language that a fuller and richer account of living things
can be given. It is curious that objections to the use of scientific
terminology often claim that it somehow 'reduces' or 'restricts' our
view of life. Exactly the reverse is the case. Explaining human or
animal life in terms of 'spirits', good or bad, is only describing them
by comparison with themselves. Scientific description allows us to
break out of our narrow prison and to show how each of the many
aspects of life can be measured and compared with the forces that can
be detected throughout the universe.

5. The influence of environment on life

Growth is the addition of material to that which is already organized
into a living pattern. But the pattern is not fixed and invariate, even
throughout any one life. Each individual changes through its lifetime,
develops, as we say, and moreover is modified by the action upon it
of its surroundings. Those parts that are exercised by the interaction
of the animal's tendencies and the surrounding circumstances increase
in amount (hypertrophy), while any disused parts undergo atrophy or
reduction. The pattern is thus able to conform to a considerable
extent to the exigencies of change in the external world. It could be
imagined that a sufficiently plastic animal organization would be able
in this way, if its tendencies to survival were strong enough, to mould
itself to all the changes of climate through the millennia, so that a
great variety of animal tvpes would arise by use and disuse alone.
Only a limited degree of change is possible in this way, however, and
it is not such changes either of development or by the direct influence
of environment that we call 'evolution'. There is abundant evidence
that the result of such interaction between organism and environment
is not handed on in the genetic code. Acquired characters are not
inherited.

8 EVOLUTION OF LIFE 1.6-

6. What is it that heredity transmit?

What is passed on is a coded pattern or plan controlling the
organization of the life processes of the next generation. The plan
takes the physical form of a series of molecules of deoxyribose
nucleotides (DNA) in the chromosomes. These by the specific
arrangements of the four types of base that they contain somehow
organize the proper linear sequences of the twenty or so amino-acids
that make up the proteins of each species. By the emergence at the
proper time during development of the appropriate proteins, enzyme
systems are produced that ensure the development and functioning of
the embryo and later the adult. We cannot fully understand how all
these processes are regulated but we see in outline how it all follows
if the DNA molecules provide a code from which natural selection
has chosen in the past those items that are suitable to provide viable
organisms for a particular environment.

The organization of life is very rarely identical in any two indi-
viduals; there is, therefore, a considerable range of potential patterns
resident in all those animals of a population that are capable of mating
together. The sum of those variants of the hereditary materials con-
stitutes the pattern or mould, as it were, of the life of the whole species.
Evolution consists in a change in this hereditary genotype, producing,
of course, a new set of adults. The genotype probably rarely stays for
long quite the same. Even in species that do not seem to be changing
rapidly there are continual adjustments, for example in the power to
produce antibodies or to manufacture enzymes. Evolution, proceeding
by mutation, recombination, and selection, is not some remote or
rare thing occurring only sporadically. It is a 'physiological' process as
much as is a change in respiration rate or in number of red cells, but
it has a longer time course than these. Evolution is the process by
which the whole population adjusts its control system to meet chang-
ing needs. Over long periods of years these adjustments produce the
new forms of life that appear as, say, the first fishes, or land animals
or mammals. Our aim is to try to discover the conditions under
which each new main group of vertebrates arose and so to understand
the processes that have been at work, modifying the basic organization.

We must therefore direct our studies continually to populations,
rather than to single individuals, thinking of all the creatures of a
kind, spread out wherever a suitable habitat for them occurs. They
will not all be alike genetically, and the circumstances of the lives of
some members of the group may become sufficiently dissimilar to

i.8 INCREASING COMPLEXITY OF LIFE 9

produce further divergences by use and disuse. Limitations of inter-
mating may occur on account of limitation of movement, accentuated
by partial and, perhaps, eventually complete geographical barriers.
Such variations in external circumstance become matched by diver-
gences in type, until two new races are produced, at first relatively
and then absolutely infertile, so that there are then two separate
populations or species instead of one.

7. The increasing complexity of life

The acquisition of new matter, and hence growth and reproduction,
occurred in the earliest animals by relatively simple means, as it still
does today in the bacteria, lower plants, and some protozoa. It is not
easy to provide rigid criteria for the definition of 'simple'; perhaps
some of the chemical changes involved may be quite complex, but the
whole system can, with meaning, be said to be simple. The number
of parts that it contains is relatively small and the number of 'adap-
tive' actions that it can take is limited. A population of bacteria in a
suitable culture medium obtains its raw materials by diffusion; the
chief device that it uses to secure these materials is to provide a large
number of spores, so that some may come to rest in suitable sur-
roundings. Such a life can be said to be more simple than that of a
vertebrate, whose system includes many special devices for obtaining
access to the raw materials that it needs. We can say that a species of
bacteria transmits less information than a vertebrate. LInfortunately
there are no satisfactory counts of the number of genes available; the
amount of DNA in bacteria is said to be about 0-05 mgm per gm
and in rat liver 2 mgm per gm. Bacteria of any one species are able to
alter their enzymes to suit the substrates available, but their life does
not depend upon the differentiation into numerous cell types each
with its special functions. The variety of information available in the
'higher' genotypes enables them to take actions that ensure survival
under conditions where the 'lower' organisms would die. Of course,
each type has its own special 'niche' and the comparison of higher and
lower is only possible if we can show exact quantitative differences.

8. The progression of life from the water to more difficult environ-
ments

In general, the new environments colonized have involved ever
wider departures from that watery one in which life first arose. This
is shown most strikingly if we contrast the simple way in which the
means of life are obtained by a marine bacterium with the complicated

io EVOLUTION OF LIFE in-

activities that go to maintain a man alive in a city. Yet all living
systems, even those that have changed most markedly since their first
origin, are still watery, and must have salt and nitrogenous com-
pounds with which to make proteins and so on. Perhaps, indeed, the
basic plan of the living activity differs less in the various types than
one might suppose. 'Protoplasm' is certainly not identical in all
creatures, but it may be that it differs less than do the outward forms
that support it.

In order to provide the conditions necessary for the maintenance of
such a watery system, in very different environments, many auxiliary
activities have been developed. It is these that give added complexity
to the higher animals and plants, enabling them to undertake what
can be called more difficult ways of life. In order to do this their
activity must also be physically greater than is necessary in more
lowly types. It may be presumed that more energy is transferred to
maintain a given mass of living matter in the less 'easy' environments,
and in this sense the higher animals are less efficient than the lower,
by a very crude criterion of efficiency.

According to this conception, then, evolution has involved a change
in the relationship between organism and environment. Life has
come to occupy places in which it did not exist before. Perhaps the
total mass of living matter has thus been greatly increased. It must
not, of course, be supposed that every evolutionary change has pro-
duced an increase in complexity in this way; examples of 'degenera-
tion' are too well known to need quoting. We have, however, a clear
impression that through the years there has been, in general, some
change in animals and plants and that in a sense some of the later
organisms are 'higher' than the earlier. It is hardly possible to deny
that there is some meaning in the assertion that man is a higher
animal than amoeba. Our thesis attempts to specify more clearly what
we can know about this evolutionary change, by saying that it con-
sists of a colonization by life of environments more and more different
from that in which life arose. This colonization was made possible
by the gradual acquisition of a store of instructions enabling adjust-
ments to be made by which life could be maintained in conditions not
tolerable before.

It is not easy to enumerate the complexity of any animal or to
define quantitatively the nature of its relations with its environment,
and for this reason it is difficult to prove our thesis rigorously. This
book nevertheless makes an attempt to show how the organization of
vertebrate life has become more complex since it first appeared, and

1.9 INVASION OF NEW ENVIRONMENTS n

that the increasing complexity is related to the adoption of modes of
life continually more remote from the simple diffusion of substances
from the sea. Of course, even the earliest vertebrates had already
departed a long way from the first conditions of life and were quite
complex organisms. However, in the history of their life through
nearly 500 million years since the Ordovician period we can trace con-
siderable further changes in complexity. During this time vertebrate
life has left the sea to live in fresh water, on swampy land, and finally
on dry land and in the air. It has produced special types able to sup-
port life by such an astonishing variety of devices that we cannot
possibly specify them all. We shall only direct attention to a few, and
thus attempt to obtain an impression of the scheme of life of the vast
hordes of vertebrate animals, which, in one shape or another, have
swarmed and still swarm in the waters and over the earth. We shall
try to discern whether there is reason to suppose that all this variety
is related in some way to changes in the surrounding world and we
may therefore finish this introduction by a brief survey of the evi-
dences for climatic and geographical changes such as may have been
responsible for the changes in organic life.

9. Changes of climate and geological periods

9.1. Changes of level of the continents

Changes of geography are mostly so slow that they cannot in them-
selves influence individual lives. On the other hand, nearly all living
things must be suited to daily and annual cyclical changes, unless they
live where no light enters. There is indirect evidence of further
changes in climate and geography, occurring with such long periods
that they are without appreciable effect on individual organisms, but
may greatly affect the history of the race.

The idea of geographical change is made familiar by the fact that
coast-lines and river-courses have changed appreciably in historical
times. We are familiar with stories of destruction of some houses or
of a village by the sea, though it may come as a shock to learn that the
sea-level has changed so much that England and France were con-
nected by land 8,000 years ago, and that man-made instruments fished
up from the Dogger Bank show that it was an inhabited peat bog
6,000 years B.C. These changes in height of the land are signs of the
'diastrophic movements', which are major features of long-period
geological evolution. The earth forces that produce these movements
are still obscure but they lead to repeated elevation and sinking of the
land masses. The action of frost, wind, and rain continually breaks up

12 EVOLUTION OF LIFE 1.9

and carries away the surface of the land, at a rate of the order of 1 ft
per 4,000 years, the processes known as weathering and denudation.
The material carried away is deposited in the river-beds and in the
lakes and shallow seas around the river mouths (sedimentation) (Fig.
1). Here it builds the sedimentary rocks, which may be many thou-
sands of feet in thickness, the whole continental platform continuing
to sink for long periods, perhaps with intervals during which it be-
comes raised above the water. Fossil remains are usually the result of

km
8

6-
4-

8,840m.

High mountain
ranges

Average height ^
r of land tr X$

\0km

Fig. i. Curve showing the areas of the earth's solid surface in relation to the
sea level. (From Holmes.)

the preservation of the harder parts of animals in sedimentary deposits,
and the most complete series of fossils are likely to be those of animals
living in the seas.

The surface crust of the earth is not a layer of uniform thickness and
density but consists of irregular masses of lighter material, rich in
silicon and aluminium (sial), forming the continents, and heavier
material, rich in magnesium (sima), under the ocean beds. The reason
for this non-uniform distribution is obscure, but it has the effect of
making the continents stand higher, floating on the plastic denser
medium beneath the crust. When material is removed from the con-
tinents by denudation they rise; conversely the addition of millions
of tons of ice will depress them. The continents are thus said to rest
in isostatic equilibrium, and following the small changes in level the
sea leaves more or less of the continental shelf uncovered. Such
upward and downward movements profoundly influence the climate.
Oceanic climatic influences tend to produce a damp, equable climate,
with large areas of marsh and forest. When the land stands higher

i. 9 GEOLOGICAL CHANGES 13

extremes of climate develop, some parts being cold, others forming
large, dry interior plains.

Besides changes in the balance produced by denudation and the
advance of ice-caps there are also from time to time marked move-
ments of uplifting or lowering of the land, which may be called
independent earth movements. Such vertical movements of the con-
tinental masses are produced by internal forces of unknown origin.
They are doubtless related to a second series of major movements of
crustal deformation that are due to tangential forces and lead to the
formation of new mountain ranges (orogenesis) by compression, or to
fracturing by tension. The upwelling of lava from the inside of the
earth at these times makes the igneous rocks, usually devoid of fossils.

Changes in geography are, then, mainly changes in the height of
the land and the amount of it that is above water. Where the con-
tinent is surrounded by a rather shallow continental shelf, this leads
to considerable changes in appearance of the land-masses. The general
opinion is that the main outline of the continental masses has remained
much as at present, at least since Cambrian times. However there have
probably been considerable movements of the land-masses in relation
to each other. Some hold that the continents of lighter material are
continually expanding, at least in certain directions, having grown
from small centres to their present size. According to the hypothesis
of Wegener, the continents have all been formed by the splitting up
of one or a few land-masses. There is indeed evidence from both
geophysics and biology that the continents have been drifting apart
(Bullard, 1959). The direction of magnetization of rocks, which is
determined at the time of their formation, shows that the land-masses
must have changed their positions greatly. For example, such data
show that during the Triassic period the British Isles lay in the tropics
and in confirmation of this we find that many salt deposits (formed
only in very warm climates) lie in the Triassic formation (Droitwich,
Bath, Nantwich, &c).

9.2. Changes of climate

Evidence of marked changes of climate is the finding in England
and other regions now temperate of animal and plant remains appro-
priate to warmer or colder conditions (corals and woolly rhinoceros,
for instance). There is thus every reason to think that there have been
great changes from hot to cold and wet to dry conditions, in conjunc-
tion with the changes in latitude and in level of the land.

These fluctuations in geography and climate are obviously of great

14 EVOLUTION OF LIFE 1.9

importance to the biologist. We can hardly expect to treat animals
and plants as stable systems if the environment around them is
changing. In order to be able to assess the influence of such changes
on life we must know more about the rates at which they occur, and
careful study shows that some of the climatic changes are rhythmic.
Rhythmic changes of climate are, of course, very familiar to us in the
cycles of days, months, and years, and the immense importance of
these short-period changes for animal and plant life must not be
forgotten.

Here we are more concerned with changes of longer periodicity, of
which the best known are fluctuations of the amount of solar radiation
received at any given part of the earth's surface. These are likely to
be especially important since plants, and hence ultimately animals,
depend for their energy on sunlight. The cycle of number of sun-
spots (n*4 years) involves a change in amount of radiation, and this is
associated with some biological cycles, for instance in the distribution
of the rings of growth made by trees. Longer-period fluctuations in
the amount of radiation received on any part of the earth's surface
depend on the perturbations of the earth's orbit, particularly on
changes in the obliquity of the ecliptic. The effect of these perturba-
tions can be calculated, and the results show that at any one place
there are rhythmical variations in the amount of radiation received,
and in its seasonal distribution. The periodicity of these calculated
changes is about 40,000 years, with considerable irregularities and
variations in the sizes of the maxima (Fig. 2).

During the last million years (the Pleistocene epoch) there has been
a series of waves of glaciation (ice ages); the ice-caps have several
times advanced towards the equator and then retreated again. These
changes are usually classified into four periods of glaciation, separated
by interglacial periods. However, the last (fourth Pleistocene) glacia-
tion, of which we know the most, certainly had three separate climaxes
of cold. The correspondence of these with especially marked minima
in the curve of solar radiation is not perfect (Fig. 2), but it suggests
that the basic periodicity may have been something like 40,000 years,
and that the division of the whole Pleistocene period into four periods
of glaciation obscures a change with much shorter periodicity. From
about 120,000 to 180,000 years b.p. (Before Present) there were no
marked minima in the solar radiation curve, and this agrees with other
evidence of a long interglacial period (third Pleistocene interglacial).
Two marked minima agree with the other signs of a penultimate (third
Pleistocene) glaciation, and this was preceded by a very long warmer

i.9 CLIMATIC CHANGES 15

period, the second inter-glacial. As we go farther back the study
becomes more and more difficult, but the available evidence suggests
that fluctuations of climate considerable enough to alter the entire
fauna and flora may have taken place at a periodicity of something
over 40,000 years. It is a measure of the difficulty of geological
science that we cannot yet give a systematic account of the chronology
or climatic changes even of the relatively recent Pleistocene period
(variously estimated at 600,000 to 1,800,000 years) during which these
glaciations occurred.

RM590 R.M550
EGI 1 EGI 2

EARLY GLACIATION

RM476 RM 435

ApGI I ApGI 2

ANFEPENULTIMATE GLACIATION

Fig. 2. Curve of solar radiation received at 65 ° N. lat. in the summer. The radiation is
expressed in 'canonic units' (related to the solar constant in calories). Time in thousands
of years. R.M. 25, &c, indicate the radiation minima. (From Zeuner, based on the tables

of Milankovitch.)

As we proceed to study times still more remote our vision becomes
increasingly blurred. We can now only rarely distinguish periodicities
as short as 40,000 years, though there is evidence that they existed, for
instance from varved Cretaceous sediments. All we can see in the
study of geological deposits are the very marked changes produced by
the major movements of orogenesis and by the isostatic readjust-
ments. The surprising thing is that these immensely slow changes
have been sufficiently regular to leave layered deposits, allowing the
development of a system of geological classification. The process of
sedimentation was interrupted by periods when the continental shelf
on which the rocks rest was raised above the water surface and under-
went denudation for a while, before being again lowered below the sea
and covered with a new deposit. During the interval, while the shelf
was raised above the water, the animals and plants in the sea became

16 EVOLUTION OF LIFE 1.9

changed; thus rather sharp breaks appear in the series of fossils. The
occurrence of these breaks has been used by geologists to define the
major geological periods, which thus correspond to cycles of elevation
and depression of the continents. By comparing the fossils contained
in the rocks major geological periods have been recognized in various
parts of the world. The times of submergence and emergence differ
from region to region, however, and no very close detailed comparison
is possible. It is easy to forget that climates and land levels do not
always change in the same direction in different parts of the world.

9.3. Geological time

Until recently most geologists assumed that there was a regular
cycle of raising and lowering (diastrophism) and that comparable
periods could be recognized everywhere. It is now widely doubted
whether there has been any such 'pulse of the earth'. The rock series
are not the same in all the continents. For example, in South Africa
three long series, known as Cape, Karoo, and Cretaceous formations,
occupy the time covered in Europe by the many elevations and depres-
sions between Silurian and Cretaceous times. Probably the conditions
under which rocks were formed have remained about the same
throughout geological time but have been interfered with by periods
of elevation, depression, and folding that are peculiar to each region.

The study of fossils often establishes the order in which the rocks
were laid down, but other methods have to be used to discover the
period of time covered by each stage. This is especially important to
the biologist, who wants to know the rate at which animals or plants
have evolved. Reliable knowledge of the ages of the rocks has only
begun to accumulate since the discovery of radioactivity. Uranium
and thorium disintegrate, producing lead, at rates that are unaffected
by any known conditions. The age of any rock since its deposition can
therefore be calculated if we can estimate the amount of breakdown
products of these elements present in it. The lead present in a rock is
often not all derived from the uranium and thorium there, but separa-
tion of the lead isotopes enables those of radioactive origin to be
estimated, and the age of the deposit can then be determined, assum-
ing that the breakdown of uranium to lead began when the rock was
crystallized in its present position. Other methods of estimating the
ages of rocks from isotope ratios have been developed. Especially
promising is the determination of the ages of the deposition of sedi-
mentary rocks from the ratio of A 40 /K 40 and Sr 87 /Rb 87 in deposits
formed by erosion of micas or granites.

1.9

GEOLOGICAL TIME

The time at which the crust of the earth assumed its present form
is now thought to have been 4,500 million years ago (Holmes, 1959)
but the rocks laid down during the greater part of this long period
contain no undoubted animal or plant remains. Cambrian rocks,
when fossils become readily discernible, were laid down about 600
million years ago.

25 60
11 40 70

MILLIONS OF YEARS
135 180 225 270 305 350 400 440

500

600

21
42

98
110

£ 161

u. 205

CEpliocene
sTl i i i
^j- MIOCENE

"IjJ-o'ugocene
~3JJeocene

235
254
2 74
300

O ,

372

412

452

PRECAMBRIAN

_i I I I I I I i l_

100

200 300 400

MILLIONS OF YEARS

500

■ ■ ' ■

600

i i i i .

50
100
150
200
250
300
350
400
450

700

Fig. 3 shows the maximum thickness of sediment in each period plotted against estimates
of the absolute date. The error attached to these determinations is shown by the
marginal lines. Apparently the rate of sedimentation has not been constant (modified

after Holmes).

Classical geology is based mainly on studies in Europe and North
America. Although a terminology based on absolute time is beginning
to emerge, it is still necessary to use that based mainly on stratigraphic
studies, begun by William Smith in the British Isles early in the nine-
teenth century. In this system, the time since the Cambrian is divided
into eleven major periods, but several of these were double or triple
periods of advance and retreat of the sea. Even the most carefully
compiled radioactivity data are not yet adequate to provide us with
definite estimates of the durations of the periods, though there is
agreement on a total period of about 600 million years since the
Cambrian. Fig. 3 shows the maximum thickness of sediment in each
period plotted against estimates of the absolute dates. The error

18 EVOLUTION OF LIFE 1.9

attached to these determinations is shown. Apparently the rate of
sedimentation has not been constant.

It is conventional to postulate a series of crustal revolutions. The
extent of the movements has not been equal throughout and some of
them, more marked than others, were times of building of great
mountain chains such as the Alps or Andes (Fig. 4). There were also
many lesser rises and falls and changes of climate with shorter periods,

Table I

MAXIMUM THICKNESSES AND REVISED TIME-SCALE

(ACCORDING TO HOLMES)

THICKNESSES IN THOUSANDS OF FEET TIME SCALE IN MILLIONS OF YEARS

WORLD
MAXIMA

CUMULATIVE

MAXIMA PERIODS

6 PLEISTOCENE

SINCE

BEGINNING

OF PERIOD

DURATION

PERIOD

15
21

21
42

PLIOCENE
MIOCENE

11
25

OLICOCENE

EOCENE

110

PALEOCENE

70 ± 2

161

CRETACEOUS

35± 5

205

JURASSIC

80 ± 5

235

TRIASSIC

25± 5

20 1 4 *
26j 46

254

300

PERMIAN

upper")
CARBONIFEROUS

LOWER J

70 ± 5

• 350 ±10

45
80

338

DEVONIAN

400 ±10

372
412

SILURIAN
ORDOVICIAN

450+10
500+15

40
60

452

CAMBRIAN

600 ±20

100

such as those of about 40,000 years that we can detect in the later part
of the Pleistocene. Many modern geologists are sceptical about the
existence of any regularities or rhythms in these changes (see Herbert,
1952, and Gilluly, 1949). It is useful when trying to adjust the mind
to periods of 30 million years to remember the frequent changes of
level and climate that have occurred in the last 100,000 years. In
spite of all that we know about the history of the earth's surface, it is
necessary every time that we make statements about the influence of
presumed climatic changes on organic evolution to remember how
scanty our knowledge is.

9.4. Classification of geological history

The period isolated as 'Cambrian' by geologists lasted 100 million
years and almost certainly included several inundations, perhaps
three. The Ordovician lasted for 60 million years and included three

i.9 RHYTHM OF GEOLOGICAL CHANGES 19

floods in North America. There were powerful earth movements at
the end of this period, at any rate in North America, known as the
Taconian revolution. The Silurian, lasting for 40 million years,
apparently included a single main cycle of inundation, ending in an
elevation of the land, which though slight in America, was marked
in Europe as the Caledonian revolution, producing the range of
mountains stretching across Scandinavia to Scotland and Ireland.

GENERALIZED CONTINENTAL

SUBMERGENCES

PALEOZOI C

ME S Z O I C

CEN0ZO1C

CAMBRIAN 0RO0VICIAN SIL DEVONIAN MISS PENN PERMIAN

h-RiAssir iiiRA«if L0W U p PER
TRIASS'C JURASSIC CRET CRETACEOUS

Tai n 1- Acadian Appalachian Nevadian Laramidt Cascadian

Fig. 4. Diagrams of main changes of areas of land and water and in climatic conditions

since the Cambrian. The chief times of mountain-building (orogenesis) in America are

also shown. (Redrawn by permission from Textbook of General Zoology, 2nd ed. by

W. C. Curtis and M. J. Guthrie, John Wiley & Sons, Inc., 1933.)

Throughout these early Palaeozoic periods the fossils are entirely
those of aquatic animals, except for some traces of land plants and
arthropods at the end of the Silurian. The oldest remains of verte-
brates are fish-scales from the Ordovician (p. 125). Details of the
Palaeozoic climatic changes are not clear, but the fact that corals,
which can now live only in warm water, were alive over a considerable
part of the earth's surface suggests that conditions were warmer than
at present at least at some early Palaeozoic times.

The Devonian is considered by some to include a single main
period, about 50 million years long, with one flood at the middle and
more arid conditions at the end, but other authorities divide it into
several periods. The first forests appeared at this time, and here, also,
are found tti3 first signs of vertebrate terrestrial life, in the form of
fossil lung-fishes and amphibians (p. 296). The period recognized as
Carboniferous in Europe includes two major periods of about 40

2o EVOLUTION OF LIFE 1.9-

million years each in America, the Mississippian and Pennsylvanian.
Throughout this long time conditions varied widely in different parts
of the world. In the early Mississippian there were many swamps in
North America. In the northern hemisphere the Pennsylvanian was
probably a time of warm, moist conditions, with no cold winters,
but there are signs that for part of this time India and Africa were
covered with an ice-sheet. The coal measures show us the remains of
the forests of spore- and seed-bearing plants that were then pro-
duced, and the land conditions evidently favoured the life of the
Amphibia.

The Permian probably constitutes a single 45-million-year period,
with very active orogenesis, leading to a more arid climate, perhaps
showing large seasonal changes, with deserts in some parts of the
world and glaciation in others. These conditions continued into the
Triassic, when the continents lay high. The reptiles, first found in
the Permian, developed throughout the Triassic and flourished in the
succeeding Jurassic period, which probably lasted 45 million years.
The Cretaceous period, during which the thick chalk deposits were
laid down, probably lasted for rather more than 60 million years,
including two major cycles of inundation. The lower Cretaceous
certainly included extensive periods of flooding, when there were
large shallow seas. Then later, towards the end of the upper Creta-
ceous, there were extensive orogenic movements, the Laramide
revolution, producing the Rockies and the Andes. The temperature
was warm until near the end of the Cretaceous, and we do not know
what condition led to the break that is found between the animals of
the Cretaceous and Eocene. Some groups of dinosaurian reptiles seem
to have died out suddenly, but it is important to notice that not all
disappeared at the same time, for instance, the stegosaurs and
pterodactyls (p. 569) disappeared well before the end of the Cretaceous.
However, it is probable that great changes went on at the end of this
period, and we may guess that a factor leading to the development of
the birds and mammals was the great rise of the continents, perhaps
accompanied by a fall in temperature over wide areas that had enjoyed
warmer weather. As always, when we look closely at such problems,
we are appalled by the vast lengths of time involved and the scanty
nature of our clues about them. The land lay very high at this time,
and the apparent abruptness of the break between Cretaceous and
Eocene fauna may be an artifact due to the scarcity of fossils. In
North America there is evidence from terrestrial deposits of a long
Paleocene period between the Cretaceous and Eocene.

i. 10 GEOLOGICAL PERIODS 21

It is usual to divide the last main geological period, the Tertiary, 1
into epochs, Paleocene, Eocene, Oligocene, Miocene, Pliocene, and
Pleistocene, the names originally referring to the percentage of fossil
genera surviving to the present day (see p. 571). Probably the whole
time since the end of the Cretaceous has been about 70 million years.
During the early part of the Tertiary period the climate was cold, but
as erosion of the mountains that had been produced at the end of the
Cretaceous proceeded the conditions became warmer, and throughout
the Eocene and Oligocene there were large forests and humid con-
ditions. Then during the Miocene there were marked earth move-
ments, leading to elevation of the land and accompanied by more arid
conditions, with wide areas of prairie and the widespread appearance
of important new food plants — the grasses. The weather probably
became gradually colder through the Pliocene, no doubt with many
fluctuations, culminating in the ice ages of the Pleistocene. Here we
come back to the period of which we have more detailed knowledge,
and are reminded that the ice age was not continuous, but interrupted
by many w r armer periods.

This very brief survey of geological history in the northern hemi-
sphere can hardly do more than remind us of the depths of our ignor-
ance. We see enough to be sure that climatic conditions have varied
throughout the millions of years, but we cannot yet see sufficient
details to allow us to discover whether there is any rhythm of major
cycles. It is easy to talk glibly of 'Carboniferous forests' or 'arid con-
ditions of the Permian', forgetting that these periods lasted for a time
that we can only roughly record in numbers and not properly imagine
in terms of our experience, although we are among the longest lived
of animals. The evidence suggests that conditions did not remain
stable for such a vast length of time as a whole geological period, but
fluctuated markedly, either irregularly or with complicated rhythms
of greater and lesser magnitude. We must not forget that very pro-
found 'climatic' changes occur every day, others every year, and some
every eleven years. It is not impossible that these shorter-period
changes, necessitating continual readjustment of animal and plant life,
have been as important as the slower changes in producing evolution.

10. Summary

To reduce to order our knowledge of vertebrate life we shall try
to discover its general organization and then examine the factors that

1 This word is a survival from an old-fashioned classification of rocks, the Tertiary heing
the period since the Cretaceous.

22 EVOLUTION OF LIFE i. 10

have produced all the varied types. The pattern of organization we
have to study is that of the animal as an active system maintaining
itself in its environment. This tendency to maintenance and growth
is the central 'force' that produces the variety of life. The opportunity
for change is provided by the fact that reproduction seldom produces
an exact copy of the parent, and thus a range of types is provided.
The tendencies to grow and to vary lead animals to colonize new en-
vironments and produce the variety of life. As evolution has proceeded
animals have come to occupy environments differing ever more widely
from the sea in which life probably arose. Life in these more difficult
environments is made possible by the development of special devices,
making the later animals more complex than the earlier and in this
sense 'higher'. It remains uncertain what influences have been respon-
sible for producing the changes in organic form. Geological evidence
shows that there have been many changes in climate and geography,
some of them proceeding at very slow rates in comparison with the
rhythms of individual animal lives. It is uncertain whether evolution-
ary changes follow these slow geological changes, or are a result of
the instability imposed on living things by climatic rhythms with
shorter periods, such as those of days, years, and the sunspot cycles.

THE GENERAL PLAN OF CHORDATE
ORGANIZATION: AMPHIOXUS

1 . The variety of chordate life

The Chordata occupy a greater variety of habitats and show more
complicated mechanisms of self-maintenance than any other group in
the whole animal kingdom. They and the arthropods and the pulmon-
ate molluscs have fully solved the problem of life on the land — which
they now dominate. This domination is achieved by most delicate
mechanisms for resisting desiccation, for providing support, and for
conducting many operations that are harder in the air than in water.
By even more wonderful devices the body temperature is raised and
kept uniform and thus all reactions accelerated. Finally, use is made of
this high rate of living for the development of the nervous system into
a most delicate instrument, allowing the animal not only to change its
response to a given stimulus from moment to moment, but also to
store up and act upon the fruits of past experience.

Besides these more developed types of chordate that dominate the
land and air there are also great numbers of extremely successful
aquatic and amphibious types. The frog is often referred to as a some-
what lowly and unsuccessful animal, but frogs and toads are found all
over the world. The sharks and bony fishes share with the squids and
whales the culminating ecological position in the food chains of the
sea, while the bony fishes are the only animals that have achieved con-
siderable size and variety in fresh water. Among the still more lowly
chordates the sea-squirts take a very important, though not dominant,
position among the animal and plant communities that occupy the
sea bottom, but they have never entered fresh water.

One could continue indefinitely with particulars of the amazing
types produced by this most adaptable phylum. Yet through all their
variety of structure the chordates show a considerable uniformity of
general plan, and there can be no doubt that they have all evolved
from a common ancestor of what might be called a 'fish-like' habit.
In the very earliest stages only the larva was fish-like, and the life-
history probably also included a sessile adult stage, such as the tuni-
cates still show today (p. 66). This bottom-living phase was then
eliminated by paedomorphosis, the larvae becoming the adults. There-
fore the essential organization of a chordate is that of a long-bodied,

24 CHORDATE ORGANIZATION n. i-

free-swimming creature. All the other types can be derived from such
an ancestor, though in some cases only by what is often called
'degeneration'.

2. Classification of chordates

We may conveniently divide the Phylum Chordata into four
subphyla :

Subphylum i. Hemichordata

Balanoglossus; Cephalodiscus; Rhabdopleura
Subphylum 2. Cephalochordata (= Acrania)

Branchiostoma
Subphylum 3. Tunicata

Ciona, Sea-squirts
Subphylum 4. Vertebrata

The Vertebrata, the largest of these groups, may be subdivided:
Subphylum Vertebrata
Superclass 1. agnatha

Class 1. Cyclostomata. Lampreys and hag- fishes

Class 2. *Cephalaspidomorphi. *Cephalaspis

Class 3. # Pteraspidomorphi. *Pteraspis

Class 4. *Anaspida. *Birkenia, *Jamoytius

Superclass 2. gnathostomata

Class 1. *Placodermi. *Acanthodes

Class 2. Elasmobranchii. Dogfishes, skates, and rays

Class 3. Actinopterygii. Bony fishes

Class 4. Crossopterygii. Lung-fishes

Class 5. Amphibia

Class 6. Reptilia

Class 7. Aves

Class 8. Mammalia.

3. Amphioxus, a generalized chordate

It has long been realized that through their great variety all these
types show certain common features, often referred to as the typical
chordate characters. It is better to regard these not as a list of isolated
'characters' but as the signs of a certain pattern of organization that
is characteristic of the group. There is much reason to suppose that
this basic chordate organization was that of a free-swimming marine
animal, probably feeding by the collection of minute particles. We
are fortunate in having still alive a little animal, amphioxus, the

ii. 3 AMPHIOXUS 25

lancelet, which shows nearly all of these features in diagrammatic form.
Study of amphioxus will go a long way to show the basic plan on which
all later chordates are built, and, indeed, gives us a strong indication
of what the early chordates must have been like.

Though it can swim freely through the water, amphioxus is essenti-
ally a burrowing animal, and many of its special features are connected
with this habitat. It lives in the sand, at small depths, and has been
found all round the oceans of the world. Evidently, in spite of its
simplicity, it is a successful type. It is found on British coasts and,
indeed, the first individual described was sent (preserved) from Corn-
wall to the German zoologist Pallas, who supposed it to be a slug and
called it Limax lanceolatus (1774). It was first figured and given the
name Amphioxus lanceolatus by Yarrell in 1836. However, the name
Branchiostoma had been given in 1834 by Costa and by the rules of
priority this is the official name of the genus. We may keep amphioxus
as a common name. Some eight species of Branchiostoma are recog-
nized, and in addition there is a group of six species referred to the
genus Asymmetron. These resemble Branchiostoma in general organi-
zation, but they have gonads only on the right side.

The adult Branchiostoma lanceolatum is rather less than 2 in. long
and has the typical fish-like organization, whose main external
features are related to the methods of locomotion and feeding (Fig.
5). The body is elongated, and flattened from side to side. The skin
has no pigment, and the muscles can be easily seen as a series of
blocks, the myotomes, serving to bend the body into folds. As the
name implies, the body is pointed at both ends; there is no recogniz-
able head separated from the body. Indeed, there are no separate eyes,
nose, or ears, and no jaws, so that the fundamental plan of chordate
organization appears in almost its fullest simplicity from one end of
the body to the other. The front end is, however, marked by a series
of buccal cirri, which form a sieve around the opening of the oral hood
and are provided with receptor cells.

Although the animal is provided with a large number of gill-slits
these do not appear externally, being covered by lateral folds of the
body, which enclose a ventral space, the atrium, opening posteriorly
by an atriopore. The outside edges of the atrium project as a pair of
metapleural folds, giving the body a triangular shape in transverse
section. The alimentary canal opens posteriorly by an anus, in front
of the hind end of the body, thus leaving a definite tail — a region of
the body not containing any part of the alimentary canal.

The general arrangement of the organs can best be understood by

26 CHORDATE ORGANIZATION n. 3-

considering the body as consisting of two tubes, the outer skin
(ectoderm) and the inner alimentary canal (endoderm), with a space
between (the coelom) lined by a third layer (the mesoderm). This
arrangement is actually found during the course of the development
(Fig. 18). The mesoderm at first forms thin layers, the somatopleure
applied to the outer body wall and the splanchnopleure to the gut.
Very soon the inner layer becomes much thickened where it is applied
to the nerve-cord and notochord, and here it forms the myotomes, or
muscle-blocks. In this dorsal part of the mesoderm the coelom,
known here as the myocoele, soon becomes obliterated, leaving the
ventral splanchnocoele around the gut. Besides the muscle that forms
in the myotomes, non-myotomal muscles develop in the somatopleure
and splanchnopleure. These are not divided into segments and are
innervated by the dorsal nerve-roots, the ventral roots supplying only
the myotomes.

4. Movement of amphioxus

The adult myotomes are blocks of striated muscle-fibres, running
along the body, separated by sheets of connective tissue, the myo-
commas. This repetition or segmentation is characteristic of the
organization of all chordates. The myocommas do not run straight
down the body from dorsal to ventral side but are V-shaped (Fig. 5).
However, each muscle-fibre runs straight from before backwards, and
the contraction of the whole myotome therefore bends the body. A
full discussion of the means by which forward motion is achieved by
such a system will be given later (p. 133). Essentially, contraction of
the myotomes results in transverse motion of the body inclined at
varying angles in such a way as to result in forward propagation. Each
myotome must therefore contract after that in front of it — the effect
being to produce an S-bend that moves backwards through the water
as the fish moves forward.

For our present purpose the point is that the contraction is serial,
that is to say, it depends on the breaking up of the longitudinal muscle
into blocks. It was probably the need for division of the musculature
that led to the development of the segmentation, and this, affecting
primarily the muscles, has come to influence a great part of chordate
organization.

Contraction of the longitudinally arranged muscle-fibres will only
produce a sharp bending of the body if there is no possibility of short-
ening of the whole. To prevent telescoping, an incompressible and
elastic rod, the notochord, runs down the centre of the body. It

II. 4

LOCOMOTION OF AMPHIOXUS

is usually stated that this is a
'supporting structure', but, of
course, an animal such as a fish in
water needs no 'support'. Nor is
the notochord a lever to which
muscles are attached, as they are
to the bones of many higher forms.
No muscles pull on it directly,
though the myocommas are at-
tached to its sheath. Its function
is to prevent the shortening of the
body that would otherwise be the
result of contraction of longitudi-
nal muscles. In fact, it serves to
make that contraction efficient in
bending the body; its elasticity
may also play an important
part.

The notochord is composed of
a series of flattened plates sur-
rounded by a fibrous sheath. The
plates are arranged in a regular
manner with their flat surfaces in
the transverse plane of the body.
They are of two sorts, fibrous
and homogeneous, which alternate
with each other. Each plate de-
velops as a highly vacuolated cell,
the nuclei being later pushed aside
to the dorsal or ventral edge. This
structure is well suited by the
turgidity of its cells enclosed in
the sheath to resist forces tending
to shorten the body. The cord of
amphioxus is peculiar in that it
extends from the very tip of the
head to the end of the tail, pro-
jecting, that is to say, beyond the
level of the myotomes, a condition
presumably associated with the
burrowing habit.

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CHORDATE ORGANIZATION

ii. 4-

Amphioxus probably does not often swim free in the water and the
body is not adapted for fast movements. It has no elaborate fins such
as those of later fishes, which ensure static stability like the feathers
on an arrow, or are movable, to allow active control of the direction

Fig. 6. Transverse section through amphioxus in the region of the pharynx.

atr. atrium; d.a. dorsal aorta; d. coel. dorsal portion of coelom; div. intestinal diverticulum;
d.n. 1 and d.n. 2 , branches of the dorsal nerve-root; end. endostyle; ep.gr. epipharyngeal groove;
/. fin-ray box; g. gonad; I y.b. primary gill bar containing coelom; my. myotome; metapl.
nietapleural fold; n. notochord; n.c. nerve-cord; ph. pharynx; sub. end. coel. subendostylar
coelom; t.b. tongue bar; v. a. ventral aorta; v.n. ventral nerve-root. (After Krause.)

of swimming (p. 136). There is a low dorsal ridge, which continues
behind as a small caudal fin. There are no definite paired fins, but the
metapleural folds might perhaps be considered comparable to the
lateral fin folds from which all vertebrate limbs are probably derived.
They are distended with coelomic fluid and, with the dorsal ridge,

II. 6

SKELETAL STRUCTURES OF AMPHIOXUS

probably serve to protect the body during the rapid dives by means of
which the creature enters the sand. The habit of swimming with the
front end downwards suggests the presence of a gravitational receptor
mechanism. The larvae of lampreys swim in a similar way (p. 114).

scut

Fig. 7. Section of the skin of amphioxus.

b.v. blood-vessel; cut. cutis; ep. epidermis; n. nerves; s.cut. sub-cutis.
(After Krause.)

5. Skeletal structures of amphioxus

Around the notochordal sheath is a further layer of gelatinous
material containing fibres. There are no cells within this material
but it is secreted by cells around the outside, which retain the epithe-
lial arrangement of the mesoderm from which they were derived.
This connective tissue continues as a sheath around the nerve-cord
and above this into a series of structures known as fin-ray boxes,
which support the median ridge. These are more numerous than the
segments and each contains a more rigid material referred to as
'cartilage'. The relationship of these structures to the fin supports of
vertebrates is obscure. Other skeletal rods occur in the cirri around
the mouth and in the gill bars.

6. Skin of amphioxus

The epidermis differs from that of vertebrates in being very thin,
composed of a single layer of cells, ciliated in the young, and with the
outer border slightly cuticularized in the adult (Fig. 7). It is not

3 o CHORDATE ORGANIZATION n.6-

known whether this cuticle contains a substance similar to the keratin
produced by the many-layered skin of later forms. There are receptor
cells but no glands or chromatophores in the skin.

Below the epidermis is a fibrous cutis, and below this again a
gelatinous material containing fibres, the sub-cutis. Both these layers
are secreted by scattered cells having some similarity to the fibroblasts

Fig. 8. Anterior end of amphioxus, from a stained and cleared preparation
of a young animal.

b.c. buccal cirri;/, fin-ray box; II. p. Hatschek's pit; my. myotome; n. notochord;
n.c. nerve-cord; p. pigment spot; ph. pharynx; v. velar tentacles; zi.o. wheel organ.

of higher forms. They contain a system of cutaneous canals, with
endothelial lining (Fig. 14).

7. Mouth and pharynx and the control of feeding

Amphioxus obtains its food by extracting small particles from a
stream of water, which it draws in by means of cilia. In all animals
that use cilia for this purpose a very large surface is provided (e.g.
lamellibranchs, ascidians), and the pharynx and gill bars of amphioxus
occupy more than one-half of the whole surface area of the body.
Special arrangements are made for the support and protection of this
ciliated surface, the wall of the pharynx being so greatly subdivided
that it needs the protection of an outer layer, the atrium.

The mouth lies covered by an oral hood whose edges are drawn out
into buccal cirri, provided with sense-cells (Fig. 8). When feeding the
cirri are curved to form a funnel-like sieve preventing the entry of
large particles. Around the mouth itself there is a further ring of

ii. 7

FEEDING OF AMPHIOXUS

sensory tentacles, the velum. The oral hood contains a complex set of
ciliated tracts, the 'wheel organ' of Miiller, and this plays a part in
sweeping the food particles into the mouth (Figs. 8 and 9). Near its
centre is a groove, Hatschek's pit, formed as an opening of the left
first coelomic sac to the exterior (p. 44).

The main operation of food collec-
tion is performed by the pharynx, a
large tube, flattened from side to side,
whose walls are perforated by nearly
200 oblique vertical slits, the number
increasing as the animal gets older.
The slits are separated by bars con-
taining skeletal rods and further sub-
division is provided by cross-bars
(synapticulae). Since the bars slope
diagonally many of them are cut in a
single transverse section, but it must
be remembered that they are essen-
tially the vertical portions of the main
walls of body and pharynx, where
these have not been perforated by a
gill-slit. Such a portion of the body
wall must contain a coelomic space
and this can in fact be seen in the
original or primary gill bars. How-
ever, an increase of the ciliary surface
is produced by downgrowth of secon-
dary or tongue bars from the upper
margin, dividing each primary slit;

these secondary bars contain no coelom. The coelomic spaces in the
primary bars, of course, communicate above and below with con-
tinuous longitudinal coelomic cavities (Fig. 6).

There are cilia on the sides and inner surfaces of the gill bars, the
lateral ones being mainly responsible for driving the water outwards
through the atrium and thereby drawing the feeding current of water
in at the mouth. In the floor of the pharynx lies the endostyle, con-
taining columns of ciliated cells, alternating with mucus-secreting
cells, which produce sticky threads in which food particles become
entangled. Various currents then draw the sticky material along until
it reaches the mid-gut. The frontal cilia of the gill bars produce an
upward current, driving the mucus from the endostyle into a median

Fig. 9. Transverse section through
front end of amphioxus.

b.c. buccal cirri; e. eyespot; H.p. Hats-
chek's pit; ?i. notochord; n.C. nerve-cord.

32 CHORDATE ORGANIZATION n. 7-

dorsal epipharyngeal groove, in which it is conducted backwards.
The cilia of the endostyle also move mucus along the peripharyngeal
ciliated tracts, behind the velum, to join the epipharyngeal groove.
Radioactive iodine is concentrated by one of the columns of the endo-
style and secreted with the mucus. Barrington (1958) suggests that
these may be regarded as the precursors of the thyroid cells, serving
to produce iodinated mucoproteins, which are then absorbed farther
down the gut (see p. 119).

The pharynx narrows at its hind end to open dorsally into a region
best known as the mid-gut, the name stomach being inappropriate.

£{■ nig. ant. fg.post (cft

/ Ag

T ^^^' |l ^ | i | Mii)iifmiTn^ r . y

Fig. 10. Currents in the mid-gut of amphioxus, showing the appearance when an
animal is placed in a medium containing carmine particles. Arrows show the chief

ciliary currents.

div. diverticulum ;f.c. food cord; h.g. hind-gut; i.c.r. ileo-colon ring; m.g.ant. and m.g.post.

anterior and posterior parts of mid-gut; oes. oesophagus. (After Barrington.)

A large mid-gut diverticulum reaches forward from this region on the
right-hand side of the pharynx. From its position this organ is often
called the liver, but Barrington has given reasons for supposing that
it is the seat of the production of digestive enzymes. Zymogen cells,
similar to those of the mid-gut, are found in its walls. Its strong dorsal
and ventral ciliation maintains in it a circulation of food materials and
secretion, and its cells are capable of phagocytosis as well as secretory
activity. Amphioxus thus combines intracellular with extracellular
digestion, doubtless in connexion with its microphagous habit.
Particles placed in the diverticulum are swept backwards and join the
main food cord that passes through the mid-gut (Fig. 10).

The hind end of the mid-gut is marked by a specially ciliated region,
the ileo-colon ring, whose cilia rotate the cord of mucus and food. The
movement is transmitted to the portion of the food cord in the mid-
gut and presumably assists in the taking up of the enzymes that
emerge from the diverticulum. Extracellular digestion takes place in
the mid-gut and the enzymes responsible have been studied by Bar-
rington. The pH of the contents varies from 67 to 7-1. An amylase is
present in extracts of the diverticulum, mid-gut, and hind-gut, but
not in those of the pharynx. Lipase and protease are present in the

ii. 8 FEEDING OF AMPHIOXUS 33

same regions, the latter having an optimum action at about pH 8-o,
being, that is to say, a tryptic type of enzyme. There is no sign of
any protease with an acid optimum, similar to the pepsin of higher
forms.

Behind the ileo-colon ring the intestine runs as a straight hind-gut
to the anus. Absorption of food takes place here, and perhaps also
in the mid-gut, apparently partly by intracellular digestion, since
ingested carmine particles are taken into the cells.

The feeding current is regulated by the rate of beat of the cilia and
the degree of contraction of the inhalent and exhalent apertures. The
walls of the atrium contain an elaborate system of afferent and
efferent nerve-fibres. The receptors include a set of large peripheral
nerve-cell bodies, lying beneath the atrial epithelium and sending
axons in by way of the dorsal roots. The motor fibres also pass through
the dorsal roots and run without synapse to the cross-striated fibres
of the pterygial muscle, which forms the floor of the atrium. The
stream flowing into the pharynx is tested by the receptors of the velum
and atrium, and if noxious material is present, the water is expelled by
closing the atriopore and contracting the pterygial muscle, producing
a 'cough'. The system can distinguish between suspensions of food
material and inorganic particles. When sufficient food has been taken,
collection is suspended until it has been digested (Bone, i960).

The atrial nervous system probably regulates spawning as well as
feeding. It has often been compared with the sympathetic system of
craniates but there are almost no close similarities. The nerve cells in
it are receptors and there is no sign of the peripheral synapse on
the efferent pathway that is so characteristic of the true autonomic
system. The atrial system is developed in relation to filter feeding
and has perhaps been completely lost in higher forms that feed by
other methods and have developed new methods to control them
(p. 117).

8. Circulation

The blood-vessels of amphioxus show in diagrammatic form the
fundamental plan on which the circulation of all chordates is based
(Fig. 11). Slow waves of contraction occur in various separate parts
in such a way as to drive the blood forwards in the ventral vessels,
backwards in the dorsal ones. Below the hind end of the pharynx
there is a large sac, the sinus venosus, into which blood from
all parts of the body is collected. From this there proceeds for-
wards a large endostylar artery (truncus arteriosus or ventral aorta)

CHORDATE ORGANIZATION

II. 8-

ant. card-

d. cuv.

d ao:

post, card'

d.ao.

from which spring vessels carrying blood up the branchial arches.
At the base of each primary bar there is a little bulb, functioning as

a branchial heart. From the gill bars
blood is collected into paired dorsal
aortae, which join behind the pha-
rynx. From the paired and median
aortae blood is carried to the system
of lacunae that supplies the tissues.
There are no true capillaries. From
the lacunae blood is collected into
veins, the most important of which
are the caudals, cardinals, and a
plexus on the gut. The cardinals are
a pair of vessels in the dorsal wall of
the coelom, and they collect blood
from the muscles and body wall.
They lead to the sinus venosus by
a pair of vessels, ductus Cuvieri,
which pass ventrally and across the
coelom to join the sinus venosus on
the floor of the gut. The caudal
veins join the plexus on the gut,
from which blood is collected by
a large subintestinal vein running
on to the liver; from here another
plexus leads to the sinus venosus.

Contractions arise independently
in the sinus venosus, branchial
bulbs, subintestinal vein, and else-
where. The rhythms are very slow
(once in two minutes), irregular,
and apparently not coordinated by
any control system.

The blood is colourless and is not
known to contain any respiratory
pigment. It contains no cells. Pre-
sumably the tension of dissolved
oxygen acquired by simple solution
is sufficient for the small energy needs of the animal, w r hich spends
most of its life at rest. It is by no means certain that any oxygenation
of the blood takes place in the gills. Orton has suggested that since

'subuit

Fig.

i i. Diagram of the circulation of
amphioxus.

aff.d. afferent vessel of diverticulum; ant.
card, anterior cardinal vein; br.a. bran-
chial arch; d.ao. dorsal aorta; d.cuv. ductus
Cuvieri; eff.d. efferent vessel of diver-
ticulum; post. card, posterior cardinal
vein; sin. sinus venosus; subint. subin-
testinal vein; v. a. ventral aorta. (After
Grobben and Zarnik.)

II. Q

EXCRETION OF AMPHIOXUS

these, through their cilia, do much of the work of the body, the
blood actually leaves the gills less rich in oxygen that when it enters
them. Oxygenation probably takes place chiefly in the lacunae close
to the skin, perhaps especially those of the metapleural folds.

9. Excretory system of amphioxus

One of the most mysterious features about the organization of
amphioxus is that there are flame-cells, comparable with those found

Fig. 12. Solenocytes of amphioxus, showing the nuclei, long flagella, and the openings
into the main excretory canal, which leads to the atrium. (After Goodrich.)

in platyhelmia, molluscs, and annelids. The excretory organs, there-
fore, do not conform to the basic chordate plan, and are in fact very
different from those not only of all other chordates but also from any
found in the remote invertebrate allies of the chordates which, as we
shall presently see, include the echinoderms, brachiopods, and polyzoa.
The nephridia lie above the pharynx. To each primary gill bar
there corresponds a sac, opening by a pore to the atrium and studded
with numerous elongated flame-cells (solenocytes) (Fig. 12). These

36 CHORDATE ORGANIZATION n. 9-

flame-cells do not open internally, but are in close contact with special
blood-vessels (glomeruli) whose walls separate the flame-cells from
the coelomic epithelium. Assuming that there are 200 of these nephri-
dia, each with 500 solenocytes 50 \x long, Goodrich, who has provided
the most accurate information about these organs, shows that the total
length available for excretion is no less than 5 metres. It is assumed
that excretion takes place by diffusion through the flame-cell wall, the
liquid being driven down the tube by cilia. Coloured particles injected
into the blood-stream are not excreted by the nephridia.

In development these remarkable organs arise from groups of cells
close to the meeting-place of ectoderm and endoderm; almost cer-
tainly they are derived from the former. They have no relation what-
ever to the mesoderm and this fact alone sufficiently indicates that
they are in no way comparable to the pronephros of vertebrates, as is
sometimes stated. There is no organ in vertebrates with which they
can be compared, nor is there any trace in amphioxus of organs com-
parable to the vertebrate kidney system. In fact we have here a
remarkable case of an isolated feature; evidently separate items of the
genotype may vary independently, and the whole bodily organization
does not necessarily change together.

The brown funnels are blind sacs at the front of the atrium,
invaginating into the epibranchial coelom. They are probably receptor
organs. Some parts of the atrial wall may perform excretory functions.
Masses of cells in the atrial floor, the atrial glands, contain granules
that may be excretory but may have been taken up from the food
current.

In the gonads, especially the testes, there are large yellow masses,
containing uric acid, which are extruded with the gametes.

10. Nervous system

Amphioxus possesses a hollow dorsal nerve-cord similar to that of
vertebrates. Though this is somewhat modified at the front end, it is
not there enlarged into an elaborate brain. The nervous system is con-
nected with the periphery by a remarkably simple set of nerve-roots,
a dorsal and a ventral on each side in each segment. The roots do not
join (Fig. 13): the ventral roots lie opposite the myotomes, to which
they carry motor-fibres, and these end on the muscle-fibres with
motor end-plates. The dorsal root runs out between the myotomes
and carries all the afferent fibres of the segment and motor-fibres for
the non-myotomal muscles of the ventral part of the body. This is the
fundamental pattern of the roots in all vertebrates.

NERVOUS SYSTEM OF AMPHIOXUS

d.n.

v.n.

Fig. 13a. Nerve-cord of amphioxus.
d.n. dorsal nerve-root; g. 'giant' nerve-fibres; v.n. ventral nerve-root. (After Retzius.)

Ret

rec

v.m.c

s.m c

median giant fibre

Fig. 13ft. Stereogram illustrating the structure of the spinal cord in an adult amphioxus.

The receptor system is made up of a more or less continuous column of bipolar cells of
Retzius (Ret.), together with smaller cells of various types (rec). According to Johnston
these receptor cells (1,2 and 3) can be regarded as equivalent to the dorsal root ganglion
cells of vertebrates. The other type of receptor cell is the giant Rohde cell (Roh.), which has
a large axon and elaborate dendritic system. It is probable that at least some of these cells
possess a peripheral axon running in the dorsal root. I.e. longitudinal connective cell.

The visceral motor cells (v.m.c.) are arranged segmentally, one per segment.

The somatic motor cells (s.m.c.) lie at a different level in the cord from the ventral
roots.

Other cells in the cord are internuncials of various types. (After Bone.)

The fibres of the peripheral nerves differ from those of vertebrates
in that they have no thick myelin sheath that will blacken with
osmium tetroxide. The nerve trunks are surrounded by an epineurium
with connective tissue cells but there seem to be no Schwann cells
accompanying the nerve-fibres (Bone, 1958).

CHORDATE ORGANIZATION

The afferent fibres of the dorsal roots are unique among chordates
in that the cell bodies are not collected into spinal ganglia but mostly
lie within the central nervous system. At least three types of central
neuron send fibres that terminate as free nerve endings in the skin. In
addition, on the head and tail there are peripheral receptor cells,
sending fibres centrally, also complicated encapsulated organs in the
metapleural folds (Bone, i960). There are numerous large multipolar
nerve-cells, presumably afferent, just beneath the atrial epithelium.

5 cut.

bucc. ep

Fig. 14. Sagittal section through the front end of amphioxus.
bucc.ep. buccal epithelium; cer. cerebral vesicle, with large nerve-cells; ep. epidermis;
my. myotome; n. notochord; p. pigment spot; s.cut. subcutis; vent, ventricle of cerebral vesicle.

(After Krause.)

These cells have many branched dendrites and an axon that runs
through a dorsal root to the spinal cord. Their status is discussed on

P-33-

The spinal cord has only a narrow lumen and its elements are

arranged as in vertebrates, namely, ependyma close to the canal, cell
layer ('grey matter'), and outer fibrous layer ('white matter'). The cells
are not arranged clearly in horns as they are in vertebrates. The most
conspicuous cells are the giant cells, which lie dorsally in the anterior
and posterior parts but are absent from about the 13th to 39th seg-
ments. Each of these cells has many dendrites, branching in the region
of entry of the dorsal root fibres, and a single axon, which runs back-
wards in the front part of the body, forwards in the hind, passing in
each case for the whole length of the cord. A median giant fibre,
which runs ventrally for the length of the cord, lies close to the
viscero-motor cells that probably produce the 'coughing' movements
of the atrium (p. 33).

II. IO

RECEPTORS OF AMPHIOXUS

Ten Cate has investigated the movements of amphioxus and found
that it responds to all stimuli by movements of 'flight'. There are no
isolated or local movements; the effect of any stimulus such as touch
on the side of the body is to produce waves of myotomal contraction.
These may, however, vary from strong waves going the whole length

g-ep.

s.ep.

p.sp.

n.pr. o.c. t.po.h

Fig. 15. Diagram of (a) the anterior end of the nervous
system of amphioxus and (b) the brain of a fish
(Polypterus).

A. Amphioxus. g.ep. granulated ependyma in the wall of the 'dorsal
central canal'; i.o. infundibular organ; p.sp. pigment spot; r.f.
Reissner's fibre in the central canal; s.ep. sensory epithelium,
u. Polypterus, a.c. anterior commissure; aq.s. aqueductus Sylvii; cer.
cerebellum; ep. epiphysis; m. medulla spinalis; n.h. neurohypophysis;
n.pr. nucleus praeopticus; o.c. optic chiasma; r.f. Reissner's fibre in
fourth ventricle; s.c.o. subcommissural organ; s.d. saccus dorsalis;
s.v. saccus vasculosus with primary sense cells; t.po.h. tractus praeop-
tico-hypophyseus. (After Olson and Wingstrand.)

of the body to single rapid twitches. The giant cells participate in the
spread of these waves. It seems likely that the arrangement ensures
that touch on the anterior part of the body, normally exposed when
feeding, produces backward movement (i.e. withdrawal into the sand)
but touch on the hind part the reverse movement of emergence and
escape.

At the front end the central canal is enlarged to form a cerebral
vesicle (Fig. 14). The whole neural tube is hardly wider here than in
the region of the spinal cord and there is no thickening of the walls,

40 CHORDATE ORGANIZATION n. 10-

which are indeed mostly formed of a single layer of ciliated epithelial
cells (Fig. 15). This is a striking indication of the lack of cephalization
of the animal. From the region of the cerebral vesicle spring the first
two dorsal roots, to which there are no corresponding ventrals. These
roots carry impulses from the receptors of the oral hood and its
tentacles.

A B C

Ifls jT^o*~r$5fc

Fig. 16. Diagram to show the direction of the eye-spots of amphioxus.
A, anterior, B, middle, and c, posterior regions of the body. The eyes are shown as if seen from
behind. D shows the direction of spiralling of the animal when swimming — as seen from in front.

(After Franz.)

The infundibular organ (Fig. 15) is composed of tall cells with long
cilia, which beat in the opposite direction to those of the rest of the
vesicle. From them fibres run backwards down the cord. The organ
is also the site of origin of Reissner's fibre (Fig. 15). This is a thread
of non-cellular material, present in all vertebrates at the centre of the
neural canal. It is secreted at the front end and then passed backwards
and is often collected and absorbed in a sac at the hind end of the
spinal cord. In vertebrates it arises from secretory ependymal cells of
the subcommissural organ, lying dorsally in the diencephalon (Fig.
1 5). The infundibular organ of amphioxus is clearly not exactly similar,
yet the Reissner's fibres are clearly comparable ; an interesting problem
in homology.

A further complication is that the cells of the infundibular organ
contain material that stains with the Gomori method, and is similar to
the neurosecretory material found in the fibres of the hypophysial tract
(Fig. 15). The organ thus seems to occupy a central position in the
control system as a receptor, originator of nerve-fibres, and of two
sorts of secretion. There is clearly much to be learned from this about
the origin and significance of the control systems of the diencephalon.

In young stages the cerebral vesicle opens by an anterior neuro-
pore, and at the point where the closure takes place there develops a
depression of the skin, lined by special epithelium, and known as
Kolliker's pit. It is said to receive no special innervation. The cells
at the front end of the cerebral vesicle contain pigment and there have

ii. ii RECEPTORS OF AMPHIOXUS 41

been attempts to show that this represents an eye. More probably
it serves to prevent rather than to receive photic stimulation; there
are other cells lying in the spinal cord that are clearly photoreceptors
(Fig. 9). In the front part of the body these are unprotected by pig-
ment, whereas more posteriorly they are so pigmented as to be pro-
tected asymmetrically from the light (Fig. 16). This asymmetry may
be connected with the fact that when swimming free in the water
amphioxus moves spirally about its axis, turning clockwise as seen
from behind. It was established by Parker that a small beam of light
produces movements of amphioxus only when it is directed on to the
region of the body or tail, not when it shines on the head. Since the
animal normally lies with the head protruding we may suppose that
the pigment spot serves to prevent light that strikes down vertically
from stimulating the photoreceptors in the cord.

Amphioxus is therefore provided with receptor and motor systems
that serve to keep it in its sedentary position, able to collect food from
the current that it makes by the cilia (p. 33). There are mechanisms
that help it to make appropriate movements of escape when it is
touched or when the body (but not head) is illuminated. The touch
receptors of the buccal cirri produce rejection of large particles and
those of the velum are chemo-receptors. The infundibular organ may
be some form of gravity or pressure receptor. By means of these
receptor organs and its simple movements of swimming, burrowing,
and closing the oral hood, the animal is maintained, probably mainly
by trial and error (phobotactic) behaviour, in an environment suitable
for its life. There are none of those elaborate mechanisms that we find
in higher chordates for 'seeking' special environments or for so
'handling' or managing them that they may prove habitable by the
animal. Amphioxus must take and leave the world very much as it
finds it. The 'correct' environment is chosen for it by the selective
settling of the larvae.

1 1 . Gonads and development of amphioxus

The gonads of amphioxus are hollow segmental sacs with no com-
mon duct. Each sac develops from mesoderm cells, perhaps originally
from a single cell, at the base of the myotomes in the branchial region,
the genital cells themselves developing on the walls (Fig. 6). The sexes
are separate and the genital products are shed by dehiscence into the
atrium, the aperture by which they escape closing and the gonad
developing afresh.

Extrusion of the gametes occurs in spring, on warm evenings

CHORDATE ORGANIZATION

following stormy weather. Fertilization is external and development
then occurs free in the water. Numerous eggs are produced and they are
small but yolky. Complex flowing movements take place in them after
fertilization, and cleavage is then rapid and complete, producing a
blastula composed of a dome of somewhat smaller and a floor of rather
larger cells (Fig. 17). These latter then invaginate to make the archen-
teron, opening by a wide blastopore, which later becomes the anus.
At about this stage the gastrula becomes covered with flagella, by
which it rotates within the egg case.

Fig. 17. Three stages in the development of amphioxus as seen in stained

preparations.
a, the blastula; b, early, and C, later gastrula.

The creature now elongates and its dorsal side flattens and eventu-
ally sinks in to form the neural tube (Fig. 18 a). At about this time
the dorsal side of the inner layer begins to fold near to the front end,
in such a way as to make a pair of lateral pouches. The walls of these
pouches are the future mesoderm and the cavity is the coelom. As in
other early chordates, therefore, the coelom is continuous at first
with the archenteron. The roof of the archenteron also arches up
dorsally and forms the notochord, the gut wall being completed by the
approximation of the edges of the remaining portion of the inner
layer, which is now the definitive gut wall or endoderm.

The analysis of the processes of development now enables us to say
something of the forces by which these formative foldings and cell
movements are produced. The formation of the neural tube, meso-
derm and notochord and the completion of the gut roof all involve an
upward movement of cells towards the mid-dorsal line. This process
of 'convergence' is a very marked feature of the development of all
chordates (Young, 1957, p. 609).

As the animal elongates, further mesodermal pouches are produced,
each separating completely from the endoderm and from its neigh-

II. II

DEVELOPMENT OF AMPHIOXUS

bours. The cells of each pouch push down ventrally on either side of
the gut, the outer ones applying themselves to the body wall to form
the somatopleure, the inner to the gut wall as splanchnopleure (Fig.
1 8 d). The inner wall of the mesoderm on either side of the nerve-
cord thickens to form the myotome, and a tongue of cells growing up
between this and the nerve-cord forms the sheaths of the latter and

lOOfJL

my coel.

som.pl.

A B C D

Fig. i 8. Further stages in the development of amphioxus as seen in transverse

sections.
A, stage of three somites; B, six somites; c, nine somites; D, eleven somites, arch, archenteron;
coel. coelom; tries, mesoderm; my. myotome; my. coel. myocoele; n. notochord; n.c. nerve-cord;
som.pl. somatopleure; spl.pl. splanchnopleure; spl.coel. splanchnic coelom. (After Hatschek.)

neurp.

g. ioo u.

Fig. 19. Young amphioxus, soon after hatching.
g. gut; «. notochord; n.c. nerve-cord; nenr.c. neurenteric canal; neur.p. neuropore.

probably also the fin-ray boxes and other 'mesenchymal' tissues. The
upper part of the coelomic cavity, the myocoele, becomes separated
from the ventral splanchnocoele. Whereas the former becomes almost
completely obliterated, the latter expands to form the adult coelom,
the cavities between the adjacent sacs breaking down.

While this differentiation of the mesoderm has been proceeding the
animal has elongated into a definitely fish-like form. The neural tube
is a small dorsal canal, opening by an anterior neuropore and con-
tinuous behind through a neurenteric canal with the gut (Fig. 19).
The larva hatches when only two segments have been formed and
swims at the sea surface by means of its ciliated epidermis, turning on
its axis from right to left as it proceeds with the front end forwards.

The mouth now appears as a circular opening and then moves
over to the left side and becomes very large. From this time onward
the whole development is markedly asymmetrical, presumably in

CHORDATE ORGANIZATION

ii. ii

connexion with the spiral movement and method of feeding. The first
gill-slit also forms near the midline but moves up on to the right side
(Fig. 20). At about the same time the right side of the pharyngeal wall
develops into a V-shaped thickening, the endostyle. Behind this there
forms a tube, the club-shaped gland, joining the pharynx to the
outside and formed by the closure of a groove in the side of the
pharynx. The significance of this organ is still obscure ; it is presum-
ably connected with the feeding process, which begins at this stage.
It has been thought to represent a gill-slit.

Fig. 20. Larval amphioxus before metamorphosis.

an. anus; c.s.g. club-shaped gland; end. endostyle; g. gill-slits lying on right

side, which will later move over to the left. H.p. Hatschek's pit (left first

coelomic sac); m. lower edge of mouth, lying on left side; n. notochord;

p. pigment spot.

The first two coelomic pouches differentiate, asymmetrically, at
this time. That on the right becomes the coelomic cavity of the head
region, while the left one acquires an opening to the exterior and a
heavily ciliated surface. This is perhaps also connected with the feed-
ing-systems and becomes developed into Hatschek's pit of the adult.
Its interest to the morphologist lies in the fact that the first coelomic
cavity opens to the exterior in other early chordates and in some
vertebrates (p. 206). The pit has thus some claim to be considered the
equivalent of the hypophyseal portion of the pituitary gland.

Further gill-slits develop in the mid-ventral line and move over on
to the right side until fourteen have been so formed. Meanwhile, a
further row of eight slits appears above that already formed. These are
the definitive slits of the right side and presently the larva proceeds to
become symmetrical by movement of eight of the first row of slits
over to the left side, the remainder disappearing. At this 'critical

ii. ii LARVA OF AMPHIOXUS 45

stage' with eight pairs of slits the larva pauses for some time before
further changes. It is interesting that this is the time at which it most
nearly represents what might have been an ancestral craniate, with
eight branchial arches (p. 145). Further slits are then gradually added
in pairs on both sides. Each slit becomes subdivided, soon after its
formation, by the downgrowth of a tongue bar. The atrium is absent
from the early larva. Metapleural folds then appear on either side and
are united from behind forwards to form a tube below the pharynx.
During the later stages of development the larva sinks and finally rests
on the bottom while undergoing the migration of gill-slits that con-
stitutes its metamorphosis. In other species the larva remains longer
in the plankton, becoming large and even showing quite large gonad
rudiments. These were at first thought to be adults of a new genus
(Amphioxides).

The development of amphioxus, like its adult organization, shows
us many features of the plan that is typical of all chordates and was
presumably present in the earliest of them. Thus the cleavage, in-
vagination, and mesoderm formation recall those of echinoderms and
other forms similar to the ancestors of the chordates, and also show a
pattern from which all later chordate development can be derived.
Unfortunately we cannot pursue this study as far as we should like
because of the difficulty of investigating the development of am-
phioxus. Modern embryologists aim at tracing the morphogenetic
movements by which the organism is built, and ultimately at dis-
covering the forces responsible for these processes. We still remain
ignorant of the details of these morphogenetic movements, and can
only guess that the system of cell activities by which an amphioxus
is built represents quite closely the original set of morphogenetic
processes of vertebrates (Young, 1957, p. 633).

There are, of course, some special features connected with the
method of life of the larva, and especially with its asymmetry. The
strange sequence of gill formation, the immense left-sided larval
mouth, perhaps the club-shaped gland, and Miiller's organ, may show
considerable modifications of relatively recent date. However, the
earliest chordates probably fed by means of cilia and were planktonic,
so we must not too hastily assume that even these asymmetrical features
are novelties.

The division of the mesoderm of amphioxus into a series of sacs
presents an interesting problem. The segmentation of the mesoderm
of vertebrates is restricted to the dorsal region. In the lowest chord-
ates (see p. 51), as in their pre-chordate ancestors, there are three

46 CHORDATE ORGANIZATION n. 11-12

coelomic cavities, but it is probable that the many segments of verte-
brates arose in order to provide a set of muscles able to contract in a
serial manner for the purpose of swimming. Their segmentation would
thus be a relatively late development, not related to the segmentation
of annelids, which divides the whole body into rings. Accordingly the
ventral part of the vertebrate coelom usually remains unsegmented.
But in amphioxus (and in the lamprey) it is subdivided from its first
appearance and only becomes continuous later. The best interpreta-
tion of this condition is to suppose that in order to provide a series of
myotomes a rhythmic process subdividing the mesoderm was adopted.
In its earliest stages this affected the whole mesoderm, ventral as well
as dorsal, but later became restricted to the dorsal region. New
morphogenetic processes may often pass through stages of refinement
and simplification in such ways.

12. Amphioxus as a generalized chordate

Amphioxus provides us, then, with a valuable example of a chordate
that retains the habit of ciliary feeding, which was probably that of the
earliest ancestors of our phylum. No doubt in connexion with this,
and the bottom-living habit, there are many specializations; the
enormously developed pharynx with its atrium, the asymmetry, and
so on; but the general arrangement of the body is almost diagram-
matically simple, and it may well be that amphioxus shows us a stage
very like that through which the ancestors of the craniates evolved.
Perhaps next the larva remained longer in the plankton and became
mature there. The Amphioxides larvae show signs of such a change.

This might give rise to a suspicion that amphioxus is not an
ancestral type but a simplified derivative of the vertebrates, perhaps
a paedomorphic form. It possesses, however, sufficient peculiar
features to make this view unlikely. Neoteny might explain the
regular segmentation, separate dorsal and ventral roots, and other
features, but can hardly account for the method of obtaining food,
for the condition of the skin, or for the presence of nephridia. It may
be, therefore, that amphioxus shows us approximately the condition
of the early fish-like chordates, living in the Silurian some 400 million
years ago, and that it has undergone relatively little change in all the
time since.

Ill

THE ORIGIN OF CHORDATES FROM FILTER
FEEDING ANIMALS

1 . Invertebrate relatives of the chordates

We have seen in the organization of amphioxus the plan of chordate
structure as it may have existed in Palaeozoic times. Before proceeding
to discuss the later forms that evolved from animals of this sort we may
first look yet farther backwards to discuss the origin of the whole
chordate phylum from still earlier ancestors. The great difficulty of
such an inquiry is itself a stimulus and a challenge. Typical fish-like
chordates were undoubtedly established by the Ordovician period,
but we have no good fossil record of their earliest form and this must
therefore be deduced from study of amphioxus and later animals. No
fossils that suggest chordate affinities have been found in the still
earlier rocks. There are, however, certain strange animals alive today
which, though not of fish-like type, show undoubted relationship with
our group. These might, of course, be degenerate offshoots from later
periods, but careful comparison suggests that they have been separa-
ted for a very long time and provide us with relics of some of the early
stages of our history.

The first step in our inquiry, however, before discussing these
forms, should be to find out, if possible, which of the main lines of
invertebrate animals shows the closest affinity with the chordates.
Almost every phylum in the animal kingdom has been suggested,
including the nemertines. Many still suppose that the annelids and
arthropods, because of their metameric segmentation, are related to
the chordates, but closer examination shows that the similarities are
superficial. The segmentation of these annulate animals is an almost
complete division of the whole body into rings, and all the organ
systems are affected by it to some extent. In chordates only the dorsal
myotomal region is segmented; even the mesoderm is not divided in
its ventral region in most animals. Moreover, the whole orientation
of the body differs in the two groups. The vertebrate nerve-cord is
dorsal to the gut, in annulates the nerve-cord is below and the 'brain'
above. The blood circulates in opposite directions, the limbs are
based on quite different plans, and so on. Attempts have been made
to get over these difficulties by turning the invertebrate upside down!
Patten and Gaskell carried such theories to extremes and tried to

48 ORIGIN OF CHORDATES in. i

show a relationship of chordates with the eurypterids, heavily ar-
moured arachnids of the Cambrian and Silurian. These animals show
a certain superficial resemblance to some early fossil fishes, the cepha-
laspids of the Devonian (Fig. 83), and these workers, with great
ingenuity, claimed to find in them evidence of the presence of many
chordate organs.

The safest evidence of affinity is a similarity of developmental pro-
cesses : animals that develop very differently are unlikely to be closely
related. The development of modern annulates is utterly different
from that of chordates. The cleavage by which the fertilized egg is
divided into blastomeres follows in annulates a 'spiral' plan, in which
every blastomere arises in a regular way and the future fate of each
can be exactly stated. In later annulates, such as the arthropods, this
plan is complicated by the presence of much yolk, but even in these
animals the cleavage does not resemble that of chordates, which is
radial or 'irregular', the cells not forming any special pattern. This
characteristic has been used to divide the whole animal kingdom into
two major groups, Spiralia and Irregularia.

The next stage of development, gastrulation, by which the ball of
cells is converted into a two-layered creature, also occurs very differ-
ently in the two groups. Our knowledge of the mechanics of the pro-
cesses by which this change is produced is still imperfect, in spite of
recent advances, but in lower chordates it occurs by invagination, the
folding in of one side of the ball of cells to form an archenteric cavity
communicating with the exterior. In annulates this is never seen;
the cells that will go to form the gut migrate inwards either at one
pole or all round the sphere and only later form themselves into a
tube, which comes to open secondarily to the outside. It is probable
that when we know more of the forces by which the gastrulation is
produced the difference will appear even more marked than it does
from this crude and formal statement that gastrulation in chordates is
by invagination, in annulates by immigration.

The same applies to the method by which the mesoderm and coelom
are formed. In lower chordates the third layer is produced by separa-
tion from the endoderm, so that the coelom is continuous with the
archenteron and is said to be an enterocoele. In annulates cells
separate in various ways to form the mesoderm and a coelom then
arises within this solid mass as a schizocoele. It is true that in some,
indeed many, of the higher chordates the coelom is never continuous
with the archenteron, but its method of development shows it to be
a modified enterocoele.

in. i INVERTEBRATE RELATIVES OF CHORDATES 49

In all these points of development the chordates differ from the
annulates, but resemble the echinoderms and their allies. Further
features support this latter relationship. One of the most important
of these is that the echinoderm-like animals, and some of the early
chordates, have a larva with longitudinal ciliated bands, very different
from the trochophore larva, in which the bands run transversely
round the body, which is found in the other line of animals. The
nervous system of annulates consists of a set of ganglionated cords,
whereas in echinoderm-like animals it is a diffuse sheet of cells and
fibres below the epidermis. The nerve-cord of the chordates can be
derived from the latter but not easily from the former condition.
Many further points could be cited, for instance, the presence of a
mesodermal skeleton in both chordates and echinoderms, but not in
annulates. It may be that there are also fundamental biochemical
differences. Most of the spirally cleaving types of animal conduct their
energy transfers with arginine phosphate, whereas vertebrates,
amphioxus, ascidians, and ophiuroid echinoderms use creatine phos-
phate. Balanoglossus and echinoids have both.

In the study of evolution it is not sufficient merely to make formal
comparisons, we must try to find out and compare the plan of develop-
ment and structure common to all members of two groups, a technique
often requiring great knowledge and good sense. When this is done in
the present case it will be found that the essential plan of development
of annulates involves spiral cleavage, gastrulation by immigration,
and a coelom formed as a schizocoele, a trochophore-like larva, and
full segmentation of the mesoderm. It is exceedingly unlikely that
such animals have given rise to chordates with their very different
development, which we may crudely define as showing radial cleavage,
gastrulation by invagination, and larva of echinoderm type.

Extending this method we may divide the whole world of Metazoa
by similar criteria into Spiralia or Polymera and Irregularia or Oligo-
mera. The former include besides the annulates the molluscs and
platyhelmia, whereas the latter group contains, in addition to the
chordates, the echinoderms, brachiopods, polyzoa (ectoprocta), grap-
tolites, pogonophora, and Phoronis. The animals in this latter group
seem at first sight to be very different from the chordates in outward
form, but the farther we look into their fundamental organization, the
more we become convinced that the ancestors of the fish-like animals
are to be found here. By study of the relics of the early chordates it is
possible to trace the history of this strange change with some plausi-
bility, though its full details will probably never be known.

ORIGIN OF CHORDATES

III. 2

2. Subphylum Hemichordata (= Stomochordata)

Class i. Enteropneusta

Balanoglossus ; Glossobalanus ; Ptychodera; Saccoglossus
Class 2. Pterobranchia

Cephalodiscus ; Rhabdopleura

Fig. 21. Balanoglossus, removed from its tube and seen from the dorsal side.
abd. abdomen; atr. atrium; an. anus; c. collar; h.c. hepatic caeca; p. proboscis; ph. pharynx.

(From van der Horst.)

Fig. 22. Balanoglossus in its tube in the sand. (After Stiasny.)

In the Hemichordata are placed animals of two types, the worm-
like Balanoglossus and its allies (Enteropneusta) and two sedentary
animals, Cephalodiscus and Rhabdopleura (Pterobranchia). The Entero-
pneusta are mostly burrowing animals (Figs. 21 and 22) varying in
different species from 2 cm to over 2 metres long. Several genera are
recognized (e.g. Balanoglossus, Saccoglossus, Ptychodera) and they
occur in all seas. Saccoglossus occurs around the British coast. The
body is soft, without rigid skeletal structures, and divided into
proboscis, collar, and trunk. The animals are very fragile and it is
difficult to collect specimens in which the hind part of the trunk

III. 2

MOVEMENT OF BALANOGLOSSUS

('abdomen') is intact. The proboscis, collar, and trunk each contain
a coelomic cavity, and the coeloms of the proboscis and collar are
distensible by intake of water through a single proboscis pore and
paired collar pores. The skin is richly ciliated all over the body. The
outer epithelium is thus unlike the squamous, layered skin of higher
forms (Fig. 23). It contains numerous gland-cells, whose secretion
is very copious, so that the animals are always covered with slime.

neur.s

Fig. 23. Section of the epidermis of an enteropneust.
h.m. basement membrane; ep. epidermal cell; gl. I and 2, different types of gland cell;
neur. neuron; neur.s. neuro-sensory cell; n.g.p. process of epidermal cell acting as neuro-
glia in the nerve net. (After Bullock, v. der Horst and Grasse.)

A characteristic feature is an unpleasant smell, resembling that of
iodoform, which possibly serves, like the mucus, as a protection.

Below the skin is a nerve plexus receiving the inner processes of
receptor cells and containing ganglion cells (Fig. 23). Deep to this are
muscles running in various directions. It is said that the animal moves
by first pushing the proboscis and collar forward through the sand
and then drawing the body after it. Protrusion of the proboscis can-
not, however, be very vigorous. It may perhaps be produced by ciliary
action distending the coelom as is usually stated — more probably by
circular muscles, but these are weak. Numerous longitudinal muscles
are present, however, in the proboscis and trunk and are partly
attached to a plate of skeletal tissue in the collar. This tissue is
attached to the ventral side of a forwardly directed diverticulum of
the pharynx. The wall of this is thick, composed of vacuolated cells,
and bears a certain resemblance to a notochord (Fig. 24). A notochord
extending throughout the length of the body would clearly be dis-
advantageous for an animal whose main movements are lengthening

ORIGIN OF CHORDATES

and shortening. It is possible that the diverticulum and plate found
in the collar represent the remains of a notochord, serving as a
fixed point by which the body is drawn forward on to the proboscis.
However, many prefer to call it a 'stomochord' to avoid too close a

card.

Fig. 24. Diagrammatic section of front end of Balanoglossus.
c. collar coelom ; card.s. sac around heart ; div. pharyngeal diverticulum ('stomochord') ; dn
dorsal nerve-root ; dv. dorsal vessel ; gl. glomerulus ; £s. gill-slit ; Im. longitudinal muscles of
proboscis ; n.c. nerve-cord ; p.p. proboscis pore ; sk. skeletal plate. (Modified after Spengel.)

comparison with the notochord. The external cilia probably play a
considerable part in locomotion; possibly they are the chief burrowing
organs, the muscles serving mainly to perform escape movements.

The mouth lies in a groove between the proboscis and collar (Fig.
25). The proboscis contains many mucus-secreting cells and the food
particles are captured on its surface and conveyed by ciliary currents
to the mouth. In the anterior part of the trunk there is a wide pharynx,
opening by a series of gill-slits (Figs. 24, 26). These resemble the
gills of amphioxus in the presence of a supporting skeleton in the gill
bars; there are also tongue bars dividing the slits from above, and

III. 2

FEEDING

Fig. 25. Feeding-currents on proboscis of Glossobalanus, shown by placing the animal

in water containing carmine particles. The particles (gra.) are either taken directly into

the mouth (?«.) as at w., or are caught up in strands of mucus (sec.) and passed backwards.

(From Barrington, Quart. J. Micr. Set. 82, by permission.)

Fig. 26. Transverse section of the pharynx of Glossobalanus.

cil. cilia of the gill bars; dc. dorsal chamber of pharynx; es. epibranchial strip; gp. gill pore;
VC. ventral chamber of pharynx. (From Barrington. With permission as for Fig. 25.)

horizontal synapticulae strengthening the gill arches. The slits open
in some species into an atrium formed by lateral folds, usually turned
upwards to leave a long mid-dorsal opening. In some species each
slit opens to a gill pouch. The whole branchial apparatus perhaps

ORIGIN OF CHORDATES

III. 2

assists in the process of feeding, probably by serving to filter off the
excess water from the material already collected on the proboscis,
which often consists of large amounts of sand or mud. Relative to the
size of the animal the pharynx is less extensive than in amphioxus,
presumably because ciliary surfaces are provided on the outside and
also large masses of sand are forced into the mouth during locomotion.
There is no endostylar apparatus, but the ventral part of the pharynx
is often partly separated from the rest (Fig. 26). Along this groove the
matter ingested is passed to a straight oesophagus and intestine open-
ing by a terminal anus. There is no true tail in the adult but a post-
anal region is present in some species during development. Numerous

v'.v. ph.

Fig. 27. Diagram of the blood system of Balanoglossus.

col. collar; d.v. dorsal vessel; glom. glomerulus; hp. hepatic caeca; m. mouth; not. 'notochord';
p. proboscis; ph. pharynx; v.v. ventral vessel. (After Bronn.)

hepatic caeca in the anterior part of the intestine can be seen from the
outside as folds of the body wall, often highly coloured.

The blood system consists of a complex set of haemocoelic spaces,
communicating with large dorsal and ventral vessels (Fig. 27).
The former enlarges into a sinus anteriorly and this is partly sur-
rounded by the wall of a pericardial cavity, which contains muscles
and may be said to be the heart, though clearly lying in a very different
position from that of other chordates. From the sinus, vessels proceed
to the proboscis and round the pharynx to the ventral vessel. The
blood is said to move forwards in the dorsal and backwards in the
ventral vessels. The front of the sinus forms a series of glomeruli,
covered by a region of the proboscis coelom specialized to form
excretory cells, the nephrocytes, some of which drop off into the
coelom. The blood is red in some species but usually colourless. It
contains a few amoebocytes.

The nervous system is one of the most interesting features of
Enteropneusta. It resembles that of echinoderms in consisting of a
sheet of nerve-fibres and cells lying beneath the epidermis all over the
body (Fig. 23). This sheet is thick in the mid-dorsal and mid-ventral

BEHAVIOUR OF BALANOGLOSSUS

lines, and in the dorsal part of the collar region it is rolled up as a
hollow neural tube, open at both ends (Fig. 24). These unmistakable
resemblances not only to the uncentralized sub-epithelial plexus of
echinoderms but also to the hollow dorsal nerve-cord of vertebrates
are most instructive, showing the affinity of the groups and the origin
of the general plan of the vertebrate nervous system. There are no
organs of special sense, unless this is
the function of a patch of special cili-
ated cells on the collar. Receptor cells
all over the body send their processes
into the nerve plexus (Fig. 23), on the
primitive plan of neurosensory cells
found elsewhere in vertebrates only in
the olfactory epithelium and the retina.
The plexus is remarkable in receiving
fibres from the outer ciliated epithelial
cells, which thus represent the epen-
dyma, the earliest form of neuroglia
(Fig. 23). Nothing is known of the
organization of pathways or of the
connexions with the muscles. The
collar nerve-cord contains giant nerve-
cells whose axons proceed backwards
to the trunk and forward to the pro-
boscis (Fig. 28). They are probably
responsible for rapid contractions
(Knight-Jones, 1951).

Bullock has investigated the beha-
viour of the animals and found only

one clear-cut reflex, namely, a contraction of the longitudinal muscles
in response to tactile stimulation. Isolated pieces of the body are able
to show reflex responses, moving away from light or tactile stimuli.
Such local actions are an interesting sign of the uncentralized nature
of the nervous system, and similar actions are found in echinoderms.
A further sign of lack of special conducting pathways is that stimula-
tion of flaps of body wall partly severed from the rest produces
generalized contraction, proving that conduction can occur in all
directions. The dorsal and ventral nerve-cords do, however, act as
quick conduction pathways, and contraction of the trunk following
stimulation of the proboscis is delayed or absent if one, and especially
if both, cords have been cut.

Fig. 28. Diagram of certain tracts in
the nervous system of Balanoglossus .

com. circular connective; col.coel. collar
coelom; col.n.c. collar nerve-cord; ep.pl.
nerve plexus in epidermis of trunk; gp.
gill pore; tr. coel. trunk coelom; tr.n.c.
trunk nerve-cord. (From Bullock, J.
Comp. Neurol., vol. 80, by permission.)

56 ORIGIN OF CHORDATES m. 2

Perhaps the most interesting behaviour observed was the activity
shown by an isolated proboscis, collar, trunk, or portion of trunk.
These organs may move around vigorously in an exploratory manner;
evidently the main nerve-cords are not necessary for the initiation of
action, as is the central nervous system of higher chordates.

There are nerve-fibres in the walls of the pharynx and oesophagus,
where peristaltic movements have been observed. Their relationship

an.

Fig. 29. Young tornaria larva, seen from the side.

an. anus; ap. apical organ; cb. longitudinal ciliated band; m. mouth;

pb. posterior ciliated band; pp. proboscis pore. (After Stiasny.)

to the rest of the nervous system is unknown. They may represent
the beginnings of an autonomic nervous system.

The sexes are separate in enteropneusts and the gonads resemble
those of amphioxus in being a series of sacs developing from cells just
outside the coelom. These proliferate and bulge into the coelom,
covered by the somatopleure. They acquire a cavity and each opens
by a narrow duct to the exterior, fertilization being external. The
development is remarkably like that of echinoderms. Cleavage is holo-
blastic and resembles that of amphioxus and ascidians, gastrulation is
by invagination, and the coelom is formed as an enterocoele, later
becoming subdivided into proboscis, collar, and trunk coeloms. Hatch-
ing occurs to produce a pelagic tornaria larva, with a ciliated band that
has exactly the relations found in the dipleurula larva of echinoderms.
The band passes in front of the mouth, down the sides of the body,
and in front of the anus (Fig. 29). It then divides into more dorsal

III. 2

DEVELOPMENT OF BALANOGLOSSUS

and ventral sections, exactly as in the production of the bipinnaria

larva of a starfish. This arrangement differs essentially from the rings

of cilia that pass round the body in the trochophore larva found in the

annelids and other spirally cleaving forms. In later tornaria larvae

there is, however, in addition to the longitudinal bands always a

posterior ring of stout cilia (telotroch), and in large oceanic forms

(which may reach 8 mm in length) the longitudinal band itself is

prolonged into prominent tentacle-like loops (Fig. 30). The cilia of

the posterior ring are purely locomotive, while those of the band set

up feeding-currents converging to the

mouth. As the larva becomes larger the

ciliary surface needed for locomotion

and feeding has to increase relatively

faster than the increasing mass of the

body, the latter following the cube but

the former only the square of the linear

dimensions. Accordingly the cilia of

the locomotive ring become broadened

and flame-like, while the convolutions

of the longitudinal (feeding) band reach

fantastic proportions. In some types,

however (Saccoglossus), the pelagic

phase is brief and the telotroch alone

is formed.

Finally the larva sinks, becomes con-
stricted into three parts, and undergoes metamorphosis into the worm-
like adult. This development is so like that of an echinoderm that it
would be necessary to consider the enteropneusts to be related to
that group even if no other clues existed. Such close similarity in
the fundamentals of development cannot be due to chance.

These animals thus provide a very remarkable and sure demonstra-
tion that the chordates are related to the echinoderms and similar
groups. The general arrangement of the nervous system as a sub-
epithelial plexus, as well as the whole course of the development, show
the affinity with the invertebrate groups, whereas the hollow dorsal
nerve-cord and the tongue-barred gill-slits are by themselves sufficient
to show affinity with the chordates, this affinity being also perhaps
suggested by other features, such as the 'notochord'. As we have seen
already, affinities are not to be determined by single 'characters' but
by the general pattern of organization of animals and especiallv that of
their development. The organization of the enteropneusts is certainly

Fig.

30. Older tornaria larva seen
from ventral surface.

Letters as Fig. 29; coel. proboscis
coelom. (After Stiasny.)

58 ORIGIN OF CHORDATES in. z-

highly specialized for their burrowing life, but showing through the
special features we can clearly see a plan that has similarity with both
the echinoderms and the chordates. The special value of study of these
animals is that it proves decisively that an affinity between these
groups exists. Exactly how they are all related is a more speculative
matter, which we shall deal with later (see p. 74).

3. Class Pterobranchia

These are small, colonial, marine, sedentary animals, which show
some signs of the general echinoderm-chordate plan of organization
we have been discussing. Cephalodiscus (Fig. 31) has been found on the
sea bottom at various depths, mainly in the southern hemisphere:
there are several species. The colony consists of a number of zooids
held together in a many-chambered gelatinous house. The zooids are
formed by a process of budding, but do not maintain continuity with
each other. Each zooid has a proboscis, collar, and trunk; there are
coeloms in each of these parts, and proboscis and collar pores. The
collar is prolonged into a number of ciliated arms, the lophophore, by
means of which the animal feeds. There is a large pharynx, opening
by a single pair of gill-slits, which serve as an outlet for the water
drawn in by the cilia of the tentacles for the purpose of bringing food.
The intestine is turned upon itself, so that the anus opens near the
mouth. A thickening in the roof of the pharynx corresponds exactly in
position with the stomochord and contains vacuolated cells. The blood
system consists of a series of spaces arranged on a plan similar to that
in Balanoglossus. There is a dorsal ganglion in the collar, but this is
not hollow. The gonads are simple sacs and development takes place
in the spaces of the gelatinous house. Gastrulation is by invagination
at least in some species and the coelom is formed as an enterocoele.
The larva somewhat resembles that of ectoproctous polyzoa, which
is not closely similar to the echinoderm larvae, but could be derived
from the same plan.

Rhabdopleura occurs in various parts of the world, including the
North Atlantic and northern part of the North Sea. The zooids are
connected together and have proboscis, collar, and trunk, ciliated
arms, coelomic spaces with pores (not 'nephridia' as is sometimes
stated) and stomochord, but no gill-slit. The development is not
known.

The Pterobranchia thus show undoubted signs of the enteropneust-
chordate plan of organization and provide also an interesting sug-
gestion of possible affinities with Polyzoa, Brachiopoda, and Phoronis.

in. 3 PTEROBRANCHS AND POLYZOANS 59

Like the Pterobranchia the Polyzoa Ectoprocta are sessile, with mouth
and anus pointing upwards. They feed by means of the cilia borne on
a horseshoe-ring of tentacles (the lophophore); but there is no division

Fig. 31. Longitudinal median section of Cephalodiscus.

a. anus; b.c. 1, 2, and 3 body cavities; int. intestine; lo. lophophore;

m. mouth; nch. 'notochord'; n.s. nervous system; oes. oesophagus;

op. operculum (collar); ov. ovary; ph. pharynx; pp. proboscis pore;

ps. proboscis; St. stomach; st.k. stalk.

(Modified after Harmer, Cambridge Natural History, Macmillan.)

into proboscis, collar, and trunk, and no tripartite coelom. The nervous
system is in the condition of a sub-epithelial plexus, which is folded,
around the base of the lophophore, to form a hollow tube — a remark-
able point of similarity to the chordates. Even though it is difficult to
compare this tube exactly with the nerve-cord of chordates, it is at
least evidence of the organization of the nervous system on a plan that
allows of such folding. It is probable that the modern pterobranchs
are the surviving members of the ancient group of graptolites, but

ORIGIN OF CHORDATES

in. 3-

mu.

gen

these are known only from the skeleton. The Pogonophora may also
be distantly related, their larva can be regarded as of tornaria type,
the coelom develops as in enteropneusts and the larval body shows
three parts, as does that of the adult in some species.

Although it would be unwise to
suggest close relationship between the
polyzoans and the pterobranchs, the
similarities are sufficient to suggest that
the chordates arose from sedentary
creatures, feeding by means of ciliated
tentacles. The evidence is sufficiently
strong to encourage us to look for the
presence somewhere in the line of verte-
brate ancestry of an animal with this
habit. The difficulties of this view arise
when we come to consider how the fish-
like organization of a free-swimming
animal first appeared, a question better
dealt with after consideration of the
tunicates.

4. Subphylum Tunicata. Sea squirts

In the adult ascidians or sea squirts
there is no obvious trace of the fish-like
form at all. The majority of these
animals are sac-like creatures living on
the sea floor and obtaining their food
by ciliary action. Often the separate
individuals are grouped together to form
large colonies, but in Ciona intestinalis,
common in British waters, the indi-
viduals occur separately, and this is possibly the primitive con-
dition for the group. The whole of the outside of the body is covered
by a tunic, in which there are only two openings, a terminal mouth and
a more or less dorsal atriopore, both carried upon siphons (Fig. 32).
The tunic is made mainly of a carbohydrate, tunicin, closely related to
cellulose, with which is combined about 20 per cent, of glycoprotein.
It is secreted by the epidermis but contains special cells that have
arrived there by migration from the mesoderm. In some tunicates
calcareous secretions of various shapes are found in the tunic. The
mantle that lines the tunic is covered by a single-layered epidermis.

Fig. 32. Diagram of structure of
Ciona.

atr.p. atriopore ; e. endostyle ; gen.d.
genital duct; h. heart; int. intestine;
m. mouth; mu. muscle; oes. oeso-
phagus; ph. pharynx; st. stomach.
(After Berrill.)

in. 4

ORGANIZATION OF CIONA

Ascidians are often brightly coloured, the pigment being either in the
tunic or the underlying body, which shows through the transparent
tunic. The colour can change, at least over a period of some days. Little
is known about the origin of the pigment, but it is sometimes derived
from the blood-pigment and may lie in pigment cells.

The mantle is provided with muscle-fibres running in various
directions but mainly longitudinally, and serving to draw the animal
together, with the production of
the jet of water from which the
animals derive their common
English name.

The greater part of the body is
made up of an immense pharynx,
beginning below the mouth and
forming a sac reaching nearly to
the base (Fig. 32). The sac is
attached to the mantle along one
side (ventral) and is surrounded
dorsally and laterally by a cavity —
the atrium. This pharynx is, of
course, the food-collecting appa-
ratus ; its walls are pierced by rows
of stigmata (gill-slits) whose cilia
set up a food current entering at
the mouth and leaving from the
atriopore. The entrance to the
pharynx is guarded by a ring of
tentacles, which may be compared

with the velum of amphioxus. The stigmata are very numerous
vertical cracks, all formed by sub-division of three original gill-
slits. Tongue bars grow down to divide each slit and then from each
tongue bar grow horizontal synapticulae. This arrangement has clear
resemblance to that of amphioxus and results in the production
of a pharyngeal wall pierced by numerous holes. Immediately within
the stigmata there is a series of papillae, provided with muscles and
cilia. There is an endostyle, which has three rows of mucus cells
on each side, separated by rows of ciliated cells and with a single
median set of cells with very long cilia (Fig. 33). The mucus secreted
in the endostyle is caught up on the papillae, whose muscles move
them rhythmically, spreading a curtain of mucus over the inside of
the pharynx. Food particles are caught in the mucus, which moves

Fig. 33. Transverse section of the endo-
style of Ciona.

lat. cil. lateral cilia; med. cil. long median cilia;
mu. mucous cell. (After Sokoloska.)

6z ORIGIN OF CHORDATES in. 4

upwards and is then passed back to the oesophagus by the cilia of a
dorsal lamina or of a series of hook-like 'languets'. Autoradiographs
made from tunicates that have been provided with isotopes of iodine
show that iodination occurs in certain cells lying above the glandular
tracts of the endostyle. Iodine is also abundant in the tunic, as it is in
the exoskeletal structures of molluscs and insects. When it became
of metabolic value its production may have become concentrated in
the pharynx (see p. 118).

The extensive ciliated surface of the pharyngeal wall ensures the
passage of large volumes of water inwards at the mouth and out at the
atriopore. Rapid change of the water is also produced by periodic
muscular contractions (p. 65). The pressure of the exhalant current is
sufficient to drive the water that has been used well away from the
animal.

The oesophagus leads to a large 'stomach' with a folded wall con-
taining gland-cells, which produce digestive enzymes. These include
much amylase, invertase, small amounts of lipase, and a protease of
the tryptic type. The organ is therefore not to be compared with the
stomach of vertebrates. A branching 'pyloric gland' opens into the
lower end of the stomach. From the stomach a rather short intestine
leads upwards to open inside the atriopore; this is apparently the
absorptive region of the gut.

The heart lies below the pharynx and is a sac, surrounded by a
pericardium (see p. 63) and communicating with a system of blood
spaces derived from the blastocoele. The larger of these spaces have
an endothelial lining; the biggest is a hypobranchial vessel below the
endostyle, from which branches pass to the pharynx. From the oppo-
site end of the heart springs a large visceral vessel and others pass to
the dorsal side of the pharynx, tunic, body wall, &c. The heart is
peculiar in that the beat can proceed in either direction. After passing
blood into the hypobranchial vessel and gills for a few beats, its direc-
tion reverses, passing the blood to the viscera. This reversal is pro-
duced by the presence of two pacemaker centres, each capable of
initiating rhythmical contractions, one at either end of the heart.
Stimulation of these by warming and cooling allows control of the
reversal of the beat. There are no capillaries and the blood system is
a haemocoele. The blood-plasma is colourless but contains corpuscles,
some of which are phagocytes, while others contain orange, green, or
blue pigment (in different species). The green and other pigments are
remarkable in that they contain vanadium. In some ascidians (Molgula)
some individuals contain vanadium, others niobium (Carlisle, 1958).

III. 4

ORGANIZATION OF CIONA

The vanadocytes contain much sulphuric acid and the metal is
associated with a chain of pyrrol rings. This haemovanadin is able to
reduce cytochrome but it remains uncertain what part the pigment
plays in respiration. The blood turns blue in air but cannot take up
more oxygen than can sea water.

The blood is isotonic with sea water, and ascidians appear to have
little or no power of regulating their osmotic pressure; none of them
is found in fresh water. They are not even able to colonize brackish
waters or those of low salinity. For example, they are rare in the
Baltic Sea, from which only six
species have been reported. Only
one species, Molgula tubifera, has
been reported from the Zuider
Zee (salinity 8-4 per mille).

A possible reason for this in-
ability to regulate the internal
composition is perhaps the need
to expose a large surface to the
water. There are no tubular ex-
cretory organs such as could be
used to maintain an osmotic
gradient. Ninety-five per cent of
the nitrogen is excreted as am-
monia. Cells known as nephro-
cytes found in the blood and
elsewhere contain concretions
within the cytoplasm and these
may in some cases be stored in an excretory sac until the animal dies.

There has been much debate as to whether the tunicates possess
a coelomic cavity. The heart develops from a plate of cells arising
early from the mesoderm and lying between ectoderm and endoderm.
This becomes grooved and folded to make the heart itself and the
pericardium. The irregular system of haemocoelomic spaces around
the pharynx and elsewhere is usually said to consist of 'mesenchyme'
and to be derived from the blastocoel and therefore not coelomic, but
its walls are mesodermal. The situation is complicated by the presence
of a pair of outpushings from the pharynx, the epicardia, or perivis-
ceral sacs, which end blindly on either side of the heart (Fig. 34).
Berrill and others have suggested that these epicardia may be com-
pared with coelomic cavities. Their function in the open condition
in which they are found in Ciona is perhaps to allow sea water to

Fig. 34. Section through base of Ciona,

showing heart, fit., in pericardium, p.,

and the epicardia, e.p., opening into the

pharynx, b.s.

at. atrium; g. gonad; int. intestine.

64 ORIGIN OF CHORDATES in. 4

circulate about the heart and hence to help excretion (and respiration ?).
In other ascidians the epicardium loses its connexion with the pharynx.
The closed sac functions in some cases as an excretory organ, con-
taining concretions of uric acid, whereas in other animals it becomes
the main source of the cells that make the asexual buds.

The central nervous system consists of a round, solid ganglion
(Fig. 36), lying above the front end of the pharynx. The ganglion has
a layer of cells around the outside and a central mass of neuropil and
is therefore quite unlike the nerve-cord of a vertebrate. From the
ganglion nerves proceed to the siphons, other parts of the mantle,
muscles, and viscera. Receptor cells with nerve-fibres ending around
the base have been described, especially in the siphons. The gut is
said to contain a plexus of cells and fibres, whose relation to the
autonomic system of higher forms remains uncertain.

Movement consists mainly of contraction and closure of the aper-
tures. Light touching of either siphon causes closure proportional to
the strength of the stimulus. Stronger stimuli cause closure of both
siphons and if very strong there is contraction of the whole body and
ejection of the water in the pharynx and atrium. Stimulation just
inside either siphon produces closure of the other one and also, if
strong enough, contraction of the body, ensuring that a jet of water
sweeps out the aperture that received the stimulus. These crossed
reflexes depend upon the integrity of the ganglion.

The surface of the body is sensitive to changes in light intensity,
and these are followed by local or total contractions, according to their
extent. After removal of the ganglion the wider reflexes can no longer
be obtained but local responses continue, suggesting the presence of
nerve-cells in the body wall. Electrical stimulation also provides evi-
dence of this. One shock may produce only a small response but if a
second shock follows shortly afterwards there is marked facilitation
and a large contraction occurs. These responses are also seen after
removal of the ganglion. The various parts of the body are not all
equally sensitive to light, the highest sensitivity being in the region
of the ganglion. The 'ocelli' are cup-like collections of orange-
pigmented cells around the siphons ; according to Hecht they are not
photoreceptors.

The neuromuscular system thus appears to function mainly as a
reflex apparatus for producing protective movements in response to
certain stimuli. This is the role that might be expected of it in an
animal that remains fixed in one place. The 'initiative' for food-
gathering activities comes from the continuous action of the cilia of

in. 4 MOVEMENTS OF ASCIDIANS 65

the pharynx. The nervous system shows little sign of those continuous
activities that produce the varied and 'spontaneous' acts of behaviour
in higher forms. Nevertheless, it would be unwise to suppose that the
nerves are only activated by external stimuli. There are some sugges-
tions that even in these simple animals rhythmical activities are
initiated from within. The food-collecting operations of the pharyn-
geal wall involve rhythmical movement of the papillae by their
muscles. Further, in many species of ascidians there are regular
contractions of the siphons and body musculature in rotation, with

Fig. 35. Rhythmical 'spontaneous' contractions of Styela shown by attaching levers

to the two siphons. Branchial siphon above, atrial siphon below. The time-marker

shows intervals of 5 minutes. (From Yamaguchi.)

a frequency of 8-27 per hour (Fig. 35). These contractions are
especially marked when the animal is in filtered water and they may
be some form of 'hunger' contraction, directed towards the obtaining
of food. More water is moved by these contractions than by the ciliary
current. Their presence is a striking warning of the dangers of assum-
ing that even the simplest nervous system operates only when
stimulated from outside.

The neural gland is a sac lying beneath the ganglion and opening
by a ciliated funnel on the roof of the pharynx. It arises mainly from
the ectoderm of the larval nervous system, in part from the pharynx.
This double embryological origin, and its position, suggest that the
neural gland may be compared with the infundibulum and hypophysis
of vertebrates. There is an obvious similarity with Hatschek's pit of
amphioxus. Both seem to be receptor organs, testing the water stream
and also producing mucus. The subneural gland has also been held
to have a similarity to the pituitary in that it controls the release of
gametes. When eggs or sperms of the same species are present in the
water, signals from the neural gland apparently produce discharge
from the gonad. The pathway of the signals is said to be partly hor-
monal, partly nervous. Discharge is produced by injection of extract of

ORIGIN OF CHORDATES

in. 4-5

neural gland or of mammalian gonadotropin, but these act through the
ganglion, since they produce no effect if the nerves leading from this
(and the dorsal strand) are cut.

Further similarities with the pituitary have been claimed, such as
the presence of vasopressor and oxytocic substances in the subneural
gland. However, oxytocin is present elsewhere in the tunicate and in

Fig. 36. Longitudinal section of the ganglion (g.) and subneural gland
(s.n.g.) of an ascidian.

cil. ciliated funnel; d.s. dorsal strand; n.a. and n.p. anterior and posterior nerves;
ph. wall of pharynx. (After L. Bertin from Grasse.)

any case differs from that of vertebrates. It cannot be claimed that the
relationship with the pituitary is clear, but it seems likely that there
is some. As in the thyroid, a pharyngeal mucus-secreting organ
stimulated by the environment has evolved into a glycoprotein-
secreting endocrine organ, controlled by substances reaching it in the
blood. (Barrington, 1959, in Gorbman, Symposium on Comparative
Endocrinology.)

5. Development of ascidians

Tunicates are hermaphrodite, the ovary and testis being sacs lying
close to the intestine and opening by ducts near the atriopore. Fer-
tilization is external in the solitary forms but internal in those that
form colonies, the development in the latter taking place within the
parent. The details of cleavage and gastrulation show a remarkable
general similarity to those of amphioxus. Indeed, the whole develop-
ment is so strikingly like that of chordates that it establishes the
affinities of the tunicates far more clearly than the vague indications

(6?)

end:

Fig. 37. Ascidian tadpole of Clavelina.

air. atriopore; c. mantle; cer.v. cerebral vesicle; e. eye-spot; end. endostyle; ep. epicardium;
h. heart; m. mouth; mu. muscle-cells; n.c. nerve-cord; not. notochord; ot. otocyst; St. stomach;

sub.n. subneural gland.

r. C. b.

Fig. 37 A. T.S. ocellus of the free swimming tadpole stage of the sea squirt Ascidia nigra.
(Drawing from an electron micrograph.)

The ocellus is situated in the posterior wall of the cerebral vesicle. It consists of three parts, a lens
cell, a pigment cell, and a retina. The lens cell usually contains three lens vesicles, which are spheres
of cytoplasm bounded by mitochondria. The pigment cell contains granules of melanin, which
protect the photoreceptor from stray light. The retinal cells have processes that penetrate the
pigment cell. They are similar to vertebral rods, composed of a pile of membranes, closely applied

to the uaner edge of the lens cell.
a. p. attachment plaque, a membrane specialization thought to function as an anchor of the retinal
cell process to the pigment cell membrane ; b.m. basement membrane, the outer limit of the cerebral
vesicle; c.v. cavity of the cerebral vesicle; I.e. lens cell; l.v. lens vesicle; m. mitochondrion; p.c.
pigment cell; p.g. pigment granule; p.m. piled menbrane of photoreceptor part of the retinal cell;
r.c.b. retinal cell body; r.c.n. retinal cell nucleus; r.c.p. retinal cell process.
(From a preparation by N. Dilly.)

68 ORIGIN OF CHORDATES in. 5-

of a chordate plan of organization seen in the adult. The result of
development is to produce a fish-like creature, the ascidian tadpole,
which is immediately recognizable as a chordate (Fig. 37). The
cleavage is total and produces a blastula with few cells, whose future

mus.c.

atr.

mus. c.

Fig. 38. The ascidian tadpole (Ascidia or Ciona type). 1. Tadpole ready to hatch.
2. Tadpole. 3. Sensory vesicle. 4. Cross section of tail.

atr. atrium; end. endostyle; fol. follicle cells; mus.c. muscle cells; mus.f. muscle fibrils;

n.c. nerve-cord; n.m. nerve to tail muscles; not. notochord; oc. ocellus; ot. otolith; su. sticking

gland; ves. sensory vesicle. (After Berrill.)

potentialities are already determined. Gastrulation by invagination
follows and the creature then proceeds to elongate into the fish-like
larva. This possesses an oval 'head' and long tail, the latter supported
by a notochord formed by cells derived from the archenteric wall.
Forty of these cells make up the entire rod, becoming vacuolated and
elongated by swelling.

On either side of this notochord run three rows of muscle-cells,
eighteen on each side, derived from mesoderm that arises from yellow-
pigmented material already visible in the egg and later forming part
of the wall of the archenteron. Other cells of this tissue migrate
ventrally to make the pericardium, heart, and mesenchyme. The

in. 6 DEVELOPMENT OF ASCIDIANS 69

muscle-cells contain cross-striated myo-fibrils at the periphery, these
being continuous from cell to cell.

The nervous system is formed by folds essentially similar to those
of vertebrates, making a hollow, dorsal tube, extending into the tail
and enlarged in front into a cerebral vesicle, within which is an
ocellus and also a unicellular otolith (Fig. 37 a). Nerve-fibres proceed
only to the front end of the rows of muscles and the rest of the cord
contains no nerve-cells or fibres (Fig. 38).

The larva takes no food and the gut is not well developed. There is
a pharynx with usually a single pair of gill-slits opening into an
atrium, which develops as an ectodermal inpushing. Below or around
the mouth various forms of sucker are formed.

The whole process of development occupies only one or two days,
and the larva, in the species in which it is set free, is positively photo-
tropic and negatively geotropic and so proceeds to the sea surface.
But its life here is also limited. Within a day or two, depending on the
conditions, its tropisms reverse so that it passes to the bottom, turns
to any dark place and thus finds a suitable surface. It attaches by the
suckers, loses its tail, develops a large pharynx, and grows into an adult
ascidian. Presumably its short life in the chordate stage is sufficient
to ensure distribution, and the simple nervous system serves to find
a place in which to live.

In addition to the sexual reproduction, tunicates have great powers
of regeneration and also often multiply by budding. The bud consists
of an outer epicardial, mesenchymal, pharyngeal or atrial tissue. The
epidermis develops only more tissue like itself and all the other tissues
are formed from the inner mass. This occurs by a process of folding
to make a central cavity; the nervous system, intestine, and peri-
cardium are then formed by further foldings. The bud thus begins in
a condition comparable to a gastrula but develops directly into an
adult, without passing through the tadpole stages. The fact that a
complete new animal is thus formed from one or two layers shows
that the separation into three layers during development does not
involve any fundamental loss of potentialities, as would be required
if the 'germ layer' theory held rigorously. The germinal tissue of the
bud is not necessarily derived from that of the parent.

6. Various forms of tunicate

Besides some 2,000 species of sessile tunicates, about 100 species
have become secondarily modified for a pelagic life. These pelagic

70 ORIGIN OF CHORDATES m. 6-

animals are perhaps all related, but the whole subphylum is con-
veniently subdivided into three classes.
Class i. Ascidiacea.

Typical bottom-living forms such as Ciona (solitary), Botryllus
(colonial).
Class 2. Thaliacea.

Pelagic forms, simple or colonial, swimming by means of circular
muscle bands. Salpa, Doliolum, Pyrosoma.
Class 3. Larvacea.

Pelagic tunicata without metamorphosis; the adult has a tail and
resembles the tadpole of the other groups. Oikopleura.

7. Class Ascidiacea

The typical sessile ascidians are found in all seas. They may be
divided into those that live as single individuals (Ascidiae simplices)
and those forming colonies (Ascidiae compositae). Both types include
many different forms, however, and the division is not along phylo-
genetic lines. The colonial forms produced by budding may consist
simply of a number of neighbouring individuals {Clavelina) or of a
common gelatinous test in which the individuals are embedded
{Botryllus, Amaroucium). The form of the body is related to the type
of bottom upon which they are found; there has thus been an adap-
tive radiation within the group; a great variety of habitats is avail-
able for bottom living creatures, and the animals become adapted
accordingly.

Most of the species live in the littoral zone, but a few deep-sea forms
are known, such as Hypobythius calycodes, found below 5,000 metres.

Many ascidians probably live only for a short time, becoming
mature in their first year and dying thereafter. In some species the
animals live over a second winter, during which they become reduced
in size, growing and budding again in the following spring (Clavelina).

8. Class Thaliacea

These are pelagic tunicates living in warm water. They have
circular bands of muscle, enabling the animal to shoot through the
water by jet propulsion. In Doliolum and its allies the muscle-bands
pass right round the body (Cyclomyaria), whereas in Salpa the rings
are incomplete (Hemimyaria). The mouth and atriopore are at
opposite ends of the body. The tunic is thin and, like the rest of the
body, transparent.

The life-history of these forms involves a remarkable alternation of

PELAGIC TUN1CATES

Fig. 39. Doliolum, gonozooid.

I, inhalent aperture; 2, ciliated pit; 3, ganglion and nerves; 4, pharynx; 5, mantle;

6, sense-cells, 7, exhalant aperture; 8, ovary; 9, intestine; 10, heart; 11, endostyle;

12, testis; 13, ciliated groove. (After Neumann.)

atr

muse

ats

br.s

Fig. 40. Cyclosalpa affinis, oozooid with chain of five wheels of blastozooids.
an. anus; atr. atrium; at.s. atrial siphon; hi. blastozooid with egg; br.s. branchial siphon; en. endo-
style; gn. ganglion; gr. gill ridge; ht. heart; muse, muscle ring; ph. pharynx; s. stomach.
( X £ modified. After Ritter and Johnson and Berrill.)

generations. In Doliolum the ascidian tadpole develops into a mother
or nurse zooid (oozooid). This by budding gives rise to a string of
daughter zooids, which it propels along by its muscles. The daughter
zooids are of three types: (i) sterile, nutritive, and respiratory indi-
viduals, the trophozooids, permanently sessile on the parent; (2)
sterile nurse forms, which are eventually set free (phorozooids); (3)
sexual forms (gonozooids, Fig. 39), nursed and carried by the phoro-
zooids until sexually mature, when they also break loose.

In Salpa the sexual form (blastozooid), produces only a single egg,

72 ORIGIN OF CHORDATES in. 8-

which develops within the mother without passing through a tadpole
stage, nourished by a diffusion placenta, whose cells also migrate into
the developing embryo. This becomes the asexual oozoid and pro-
duces a long chain of blastozooids, which it tows about until these
break away by sections (Fig. 40).

The pelagic colonial Pyrosoma of warm seas consists of a number of
individuals associated to form an elongated barrel-shaped colony.
The mouths open outwards and the atria inwards into a single
cavity with a terminal outlet from which a continuous jet emerges.

The mode of budding from the epicardium
and other features suggest an affinity with
Doliolum and Salpa, but Pyrosoma also
resembles the ascidians in that its zooids
are all sexual and capable of budding. The
yolky eggs develop within the parent,
without forming a larva. The outstanding
characteristic of the creatures is the
powerful light that they shine. This is
Fig. 41. Photogenic cell of produced in photogenic organs on each

Pyrosoma. (After Kukenthal.) r . r mi 1

side or the pharynx. 1 he photogenic cells
contain curved inclusions about 2^ in diameter (Fig. 41). These
are considered by some to be symbiotic luminescent bacteria, but
this is doubtful. The light is so powerful that when large masses of
Pyrosoma occur together the whole sea is illuminated sufficiently to
allow of reading a book. A remarkable feature of the phenomenon
is that the light is not produced continuously but only when the animal
is stimulated, as by the waves of a rough sea. If one individual is
stimulated others throughout the colony may show their lights, but
the mechanism of this effect is not known and the groups of cells that
form the luminescent organs receive no nerves. Other types of animal
with luminescent bacteria emit light continuously. The sudden flashes
of light probably serve as a dymantic reaction (p. 302), giving protec-
tion against enemies by producing a flight-reaction in the same way
as do sudden manifestations of colour or black spots by other animals.
It has been observed in the laboratory that colonies of Pyrosoma that
are dying and do not light up may be eaten by fishes, whereas any
that light up when seized may then be dropped.

9. Class Larvacea

The (Appendicularia) Larvacea (Figs. 42 and 43) are minute neo-
tenous tunicates that live in the plankton. Instead of the test, each

ill. 9

LARVACEA

Fig. 42. Oikopleura, one of the Larvacea, in its house, showing

the feeding-currents.

e. exhalant aperture; e.e. 'emergency exit'; f. p. filter pipes; f.tv. filter

window; g. gill-slit; m. mouth; r. trough; ta. tail. (After Garstang;

this and Figs. 44 and 45 by permission of the Editors of the Quarterly

Journal of Microscopical Science.)

individual builds a 'house', by secretion from a special part of the skin,
the 'oikoplastic epithelium'. The tail is a broad structure held at an
angle to the rest of the body; its
movement produces a current in
which the food is carried and caught
by a most elaborate filter arrangement
ixi the house (Fig. 42). Water enters
the house by a pair of posterior
'filtering windows' and is passed
through a system of filter pipes in the
part of the house in front of the
mouth. The very minute flagellates
of the nanonplankton are stopped by
these pipes and sucked back to the
mouth. The pharynx has two gill-slits,
also an endostyle and peripharyngeal
bands. The general organization is that
of a typical ascidian tadpole, and there
can be no doubt that these forms have
arisen from tunicates by the accelera-
tion of the rate of development of the
alimentary organs and gonads so that
the metamorphosis and normal adult
stage are eliminated. This may, of
course, have happened long ago, so
that the modern Larvacea are not FlG - «■ Appendicular* t seen from

the side and from below.

closely related to any living forms, (After Lehmann.)

74 ORIGIN OF CHORDATES in. 9-

but the fact that they differ in many ways from known ascidian
tadpoles does not invalidate the hypothesis; it would be expected
that many special features would be developed during evolution
after the paedomorphosis. Garstang, however, believed that there
is sufficient evidence to show that the Larvacea are related to the
Doliolidae and suggested an ingenious hypothesis by which the appendi-
cularian home could be derived from the doliolid test, the animal
itself remaining attached at the front end by gelatinous threads, which
came to make the filter tubes (Fig. 44).

Fig. 44. Sequence of stages by which the Larvacea may have
been evolved from a doliolid type.

A, Thaliaccan type of individual in its test (t). b, Paedomorphosis has
occurred so that a tailed creature is found in the test; g. gill-slit, c, The
tadpole has moved away from the inhalant aperture, leaving a series
of threads that become the filter pipes (/./>.), the inhalant aperture
becoming exhalant and vice versa. (After Garstang.)

The tail is a highly developed organ, serving for locomotion, nutri-
tion, and in the building of the house. It has a wide, continuous fin
and is supported by a notochord of 20 cells. Bands of 10 large striped
muscle-cells extend down each side, giving an appearance that has
been compared with metameric segmentation. The small number of
the cells makes any such comparison very difficult. Moreover, the
muscles are not developed from anything resembling myotomes. The
nerve-cord is a hollow tube with ganglionic thickenings, each con-
taining one to four nerve-cells. From these cells fibres proceed to
the muscles and to the skin in a series of roots that usually remain
separate, the motor being more dorsal.

10. The formation of the chordates

We can now recapitulate the points that we have established about
the origin of the chordates and attempt to piece together the evidence
to show the sequence of events that led to the production of a free-

in. 10 LARVAL ANCESTRY OF CHORDATES 75

swimming, fish-like animal. The chordates are related to the echino-
derms and their allies. This is established by the similarities in early
development (cleavage, gastrulation, mesoderm formation); by the
presence in early members of both groups of three separate coelomic
cavities, some with pores; by the similarity of the larva of entero-
pneusts to the dipleurula, and by other points of general morphological
and biochemical similarity between early chordates and echinoderms,
especially the arrangement of the nervous system and presence of a
mesodermal skeleton.

The echinoderms we have to consider are not the modern star-
fishes and sea-urchins, which are relatively active animals, but their
sessile Palaeozoic ancestors. These were sedentary, often stalked
animals, the cystoids, blastoids, and crinoids, feeding by ciliary
action. Surviving animals of related phyla, such as Polyzoa Ecto-
procta and Phoronis suggest that the ancestor for which we are looking
may have possessed a ciliated lophophore for food-collecting. For
purposes of dispersal its life-history presumably included a larval
stage with a longitudinal ciliated band, similar in plan to that of the
auricularia.

One might well ask how such an animal could possibly become
converted into a motile, metameric fish, feeding with its pharynx.
Yet the evidence of the lower chordates is sufficient to establish that
this change has occurred, and even provides us with an outline of the
main stages in the process of the change. Cephalodiscas, which is in
some ways the most primitive of surviving chordates, with its lopho-
phore also possesses gill-slits. This suggests that the pharyngeal
mechanism was substituted for the lophophore as a means of feeding
in the adult stage. There are other possible interpretations. It has
been suggested that Cephalodiscus was derived from a larval entero-
pneust (Burden-Jones). However, it is possible that ciliary mechanisms
developed in the pharynx first to deal with food collected outside by
tentacles or proboscis. Later the pharynx became developed into a
self-contained feeding mechanism, making unnecessary the tentacles,
which provide a tempting morsel for predators. The adoral band of
cilia of the auricularia probably serves to carry food into the mouth,
and for this purpose it is actually turned in to the floor of the pharynx.
Garstang suggests that the endostyle has been derived from this loop
of the adoral band.

The pharyngeal method of food-collecting thus replaced the ten-
tacles in the adult and the whole apparatus of an endostyle and an
atrium to protect the gills became developed. We may notice here the

7 6

ORIGIN OF CHORDATES

III. 10

remarkable similarity of this arrangement of the pharynx in tunicates,
amphioxus, and cyclostome larvae, and the partial similarity in
Balanoglossus.

The tunicates show us a stage in which branchial feeding has fully
replaced tentacle feeding in a sessile adult. But they have a larva that
is beyond all question a fish-like chordate. If the adult tunicate has
evolved from a modified lophophore-feeding creature, how has the

Fig. 45. To show the method by which a protochordate animal might have been

derived from an echinoderm larva such as the auricularia.

a. Auricularia in side view; b. protochordate in side view; c. same, dorsal view. ad.b. adoral

band; an. anus; coel. coelom; end. endostyle; g. gill-slit; Lb. longitudinal ciliated band;

m. mouth; n.c. nerve-cord; not. notochord. (After Garstang.)

ascidian tadpole arisen from the auricularia larva ? Garstang's auri-
cularia theory, first propounded in 1894, provides a possible answer.
As a ciliated larva grows its means of locomotion becomes inadequate
because the ciliated surface increases only as the square of the linear
dimensions, the weight as the cube. Muscular locomotion is not sub-
ject to this difficulty, and some of the starfish larvae actually show
flapping of the elongated processes, movements that presumably
assist them to remain at the surface. Garstang suggests that the fish-
like form arose by development of muscles along the sides of the
elongated body, the ciliated bands being pushed upwards and even-
tually rolled up with their underlying sheets of nerve plexus to form
the neural tube. The adoral ciliated band might then well be the
endostyle (Fig. 45).

This theory may seem at first sight fantastic. It is necessarily
speculative, but it has certain strong marks of inherent probability. It

in. 10 LARVAL ANCESTRY OF CHORDATES 77

violates no established morphological principles and certainly enables
us to see how a ciliated auricularia-like larva could be converted by
progressive stages into a fish-like creature with muscular locomotion,
while the adults, at first sedentary, substituted gill-slits and endostyle
for the original lophophore. The alternative is to suppose that the
ascidian tadpole arose as a purely tunicate development, providing
sufficient receptor and muscular organs to allow for the finding of
suitable sites on the bottom (Berrill, 1955).

We may plausibly regard the adult tunicate organization as directly
derived from that of sessile lophophore-feeding creatures, and the
larval organization as descended from an echinoderm-like larva.
There is no need, on this view, to regard the sessile adult tunicate
as a 'degenerate' chordate. The problem that remains is in fact not
'How have sea-squirts been formed from vertebrates ?' but 'How have
vertebrates eliminated the sea-squirt stage from their life-history?'
It is wholly reasonable to consider that this has been accomplished by
paedomorphosis. Advance of the time of development of the gonads
relative to that of the soma is well known to occur in certain special
cases such as the axolotl. The example of the Appendicularia shows
that a similar process can happen among tunicates! Various workers
have stressed the differences between the ascidian tadpole and the
adult appendicularian, in attempts to show that the two are not
comparable. But the differences, though considerable, are superficial :
the similarity of organization is profound. Any sensible biologist with
an understanding of the way in which the characteristic forms of
animals arise by change in the rate and degree of development of
features can see how the Appendicularia may represent modified
ascidian larvae.

The appendicularians do, indeed, carry certain characters of the
'adult' sea-squirt, in particular they have gill-slits, though of simple
form. Nothing is more likely, however, than that some features of the
sessile adult would be adumbrated in its larva and capable of fuller
development therein if advantageous. Larva and adult, it must be
remembered, possess the same genotype; the remarkable feature in all
animals with metamorphosis is the difference between the two stages,
not the similarity. Any characteristic may appear at either larval or
adult stage or be transferred by evolutionary selection from one to the
other. There is no serious objection to the view that the early adult
free-swimming chordates arose by paedomorphosis of some tunicate-
like metamorphosing form. If the creatures abandoned the habit
of fixation it would be possible for characters previously present

78 ORIGIN OF CHORDATES in. 10

separately in larva and adult to become combined in a single stage.
This is indeed what has happened in the Appendicularia.

Strangely enough, one of the chief difficulties of this theory is to
find the position of the enteropneusts. Since the larva is still in the
ciliated-band stage there should be no sign of organs characteristic of
the muscle-swimming, fish-like pro-chordate. Yet such signs are
present in the adult Balanoglossiis; there is a hollow nerve-cord and
some sign of a notochord. These features almost compel us to suppose
that the group has at one time possessed a free-swimming, fish-like
stage. The only escape from this conclusion would be by supposing
the hollow nerve-tube to be a case of convergence, for which a parallel
might be cited in the hollow nervous system of Polyzoa. But there is
no clear reason why the nerve-cord should become rolled up in the
collar, and it is easier to suppose it a vestige. This imposes two further
hypotheses on us. First that a fish-like stage once followed an advanced
ciliated-band stage in ontogeny, and secondly that this fish-like stage
later became adapted to a burrowing life, in fact that Balanoglossus is
a 'degenerate' chordate. Neither of these propositions is impossible,
but it must be admitted that the position of the enteropneusts is not
clear. Showing a combination of ciliated larva and chordate characters
they provide a valuable proof of the affinity of chordates and echino-
derm-like creatures, but these very chordate characters become an
embarrassment when we try to explain in detail how they have arisen!

There is strong reason to suppose that what we may call the Bate-
son-Garstang theory of the origin of chordates is correct. There is little
doubt that chordates are related to the sessile lophophore-feeding
type of creature rather than to any annulate, and we can reconstruct
the course of events by which the lophophore-feeder may have come
to have a pharynx with gill-slits and its larva to have muscles, a noto-
chord, and a nerve-tube. Then by paedomorphosis the sessile stage
disappeared and the free chordates began their course of evolution.
There are some reasons for supposing that a type such as amphioxus
could have been derived from a creature not distantly related to the
simpler Appendicularia and this in turn from a neotenous doliolid or
some similar ancestral type.

We need not, however, follow the theory into its details, which are
speculative. The whole treatment provides a conspicuous example
of close morphological reasoning, allied with proper consideration of
general biological principles, and establishes with some probability
the main outlines of the origin of our great phylum of active creatures
from such humble sedentary beginnings.

80 ORIGIN OF CHORDATES in. 10

Can we see in the production of the first fish-like creatures clear
signs of an 'advance' in evolution ? In acquiring the power of active
muscular locomotion the animals became able to live and feed in a
variety of habitats, either at the sea surface or on the bottom. Forms
with a sedentary adult stage are limited by the necessity for the
presence of a sea bottom of suitable character. The larvae were evolved
to provide the information to make sure of reaching such conditions.
But whereas suitable situations on the bottom are not common, and
are liable to change, the sea surface provides a generalized habitat in
which there is always abundant food, though no doubt also strenuous
competition for it. Paedomorphosis in this case, as in others, allows
the race to eliminate from its life-history the stage passed in a 'special'
environment, which is difficult to find. Although the fish-form that
was thus produced proved to have great possibilities for further
evolution, the change was not at first a strikingly progressive one.
The surface of the sea is perhaps the most general of all environments ;
possibly it was the seat of the origin of life. Races that have devised
means of living on the sea bottom may therefore be said to have
advanced, because they have invaded a more difficult habitat. To
abandon the sedentary life might in this sense be regarded as a retro-
grade step. The peculiar feature of the early fishes, however, was that
they developed powers of active movement in a relatively large
organism provided with efficient receptors, and by making use of the
feeding mechanism developed at first by the bottom-living adult were
able to live successfully at the sea surface. They acquired their
dominance at this stage not by invading new habitats but by develop-
ing effective means of living in the richly populated plankton.

THE VERTEBRATES WITHOUT JAWS. LAMPREYS

1. Classification

Phylum Chordata

Subphylum 4. Vertebrata (= Craniata)
Superclass 1. Agnatha
Class 1. Cyclostomata
Order 1. Petromyzontia

Petromyzon; Lampetra; Entosphenus; Geotria; Mordacia
Order 2. Myxinoidea
Myxine; Bdellostoma

Class 2. *Osteostraci. Silurian-Devonian
*Cephalaspis; * Tremataspis

Class 3. *Anaspida. Silurian-Devonian
*Birkenia; *Ja?noytius

Class 4. *Heterostraci. Ordovician-Devonian
*Astraspis; *Pteraspis; *Drepanaspis

Class 5. *Coelolepida. Silurian-Devonian.
*Thelodus; *Lanarkia

Superclass 2. Gnathostomata

2. General features of vertebrates

All the remaining chordates are alike in possessing some form of
cranium and some trace of vertebrae; they make up the great sub-
phylum Vertebrata, also called Craniata. The organization of a verte-
brate is similar to that of amphioxus, but with the addition of certain
special features. A few of these novelties may now be surveyed, with
emphasis on those that provide the basis for the capacity to live in
difficult environments that is so characteristic of the vertebrates.
Firstly the front end of the nervous system is differentiated into an
elaborate brain, associated with special receptors, the nose, eye,
and ear. Through these receptors the vertebrates are able to respond
to more varied aspects of the environment than are any other animals.
Some of them have the ability to discriminate between visual shapes
and colours, and in the auditory field between patterns of tones, also
between a host of chemical substances. The motor organization
allows the performance of delicate movements to suit the situations

82 VERTEBRATES WITHOUT JAWS iv. 2-

that the receptors reveal. The swimming process, by the passage
of waves down the body, is itself perfected by improvements in the
shape of the fish, allowing rapid movements and turns. Besides the
median fins there develop lateral paired ones, serving at first a
stabilizing and steering function and then converted, when the land
animals arose, into organs of locomotion on the ground or in the air
and finally, in the shape of the hands, into a means of altering the
environment to suit the individual.

The brain itself, at first mostly devoted to the details of sensory
and motor function, comes increasingly to preside, as it were, over
all the bodily functions, and to give to the vertebrates the 'drive' that
is one of their most characteristic features. The skull is developed as
a skeletal thickening around the brain, probably at first mainly for
protection, but later serving for the attachment of elaborate muscle
systems. The study of vertebrates is especially identified with study
of the skull, because in so many fossils this is the only organ preserved.

The food of the earliest vertebrates was collected by ciliary action,
but this habit has long been abandoned and only in rare cases today
does the food consist of minute organisms. The pharynx of most
vertebrates is small, there are relatively few gill-slits and these are
respiratory. In all except the most ancient forms the more anterior of
the arches between the gills became modified to form jaws, serving not
only to seize and hold the food but also to 'manipulate' the environ-
ment.

The blood system shows two of the most characteristic vertebrate
features, namely, the presence of a heart that has at least three
chambers and thus provides a rapid circulation, and of haemoglobin
within corpuscles, serving to carry large amounts of oxygen to the
tissues. The efficiency of this system must have been a major factor
in producing the dominance of the vertebrate animals. In the air-
breathing forms, and especially the warm-blooded birds and mam-
mals, the respiratory and circulatory systems allow the expenditure of
great amounts of energy per unit mass of animal, so that quite extra-
vagant devices can be used, allowing survival under conditions that
would otherwise not support life.

The excretory system is based on a plan quite different from that
of amphioxus. It consists of mesodermal funnels, leading primarily
from the coelom to the exterior. It may be that this type of kidney
arose in connexion with the abandoning of the sea for fresh water.
Probably all but the earliest vertebrates have passed through a fresh-
water stage, and it is significant that all except Myxine have less salt in

iv. 4 AGNATHA 83

their blood than there is in sea water. Elaborate devices for regulation
of osmotic pressure have been developed, and the mesodermal kidneys
play a large part in this regulation.

This outline only gives a few suggestive features of vertebrate
organization. The details differ bewilderingly in the different types
and it is our business now to survey them. In the earliest forms the
more special mechanisms are absent or at least function only crudely,
and passing through the vertebrate series we find more and more
devices adopted, along with more and more delicate co-ordination
between the various parts, culminating in the extremely highly
centralized control of almost every aspect of life that is exercised by
the mammalian cerebral cortex.

3. Agnatha

The earliest vertebrates, while showing most of the characteristic
features of the group, differ from the rest in the absence of jaws and
are therefore grouped together in a superclass Agnatha, distinguished
from the remaining vertebrates, which have jaws, and are therefore
called Gnathostomata. The only living agnathous animals are the
Cyclostomata, lampreys and hag-fishes, but the first vertebrates to
appear in the fossil series, mostly heavily armoured and hence known
as 'ostracoderms', found in Silurian and Devonian strata, also show
the agnathous condition, and have some other features in common
with the Cyclostomata. This group of agnathous vertebrates shows
some interesting experimentation in methods of feeding, before the
jaw-method became adopted. The modern cyclostomes are parasites
or scavengers, in the adult state, but as larvae the lampreys still feed
on microscopic material, using an endostyle resembling that of
amphioxus in many ways, but making use of muscular contraction
rather than ciliary action to produce a feeding current. The methods
of feeding of the Devonian forms are not known for certain, but
probably included shovelling detritus from the bottom.

The Cyclostomata are therefore worth special study as likely to
show us some of the characteristics possessed by the earliest vertebrate
populations.

4. Lampreys

The most familiar cyclostomes are the lampreys, of which there are
various sorts found in the temperate zones of both hemispheres. All
lampreys have a life-history that includes two distinct stages: the
ammocoete larva lives in fresh water, buried in the mud, and is

8 4 VERTEBRATES WITHOUT JAWS iv. 4-

microphagous: the adult lamprey has a sucking mouth, and usually
lives in the sea, where it feeds on other fishes. Lampetra the lamprey
(Fig. 47), is a typical example, common in Great Britain. The adult
is an eel-like animal about 30 cm long, black on the back, and white
below. The surface is smooth, with no scales. The skin is many-
layered (Fig. 48). The outermost cells have a striated cuticular border.
Mixed with these epithelial cells the lamprey, like most aquatic
vertebrates, has many gland-cells for producing slime. Below the
epidermis lies the dermis, a layer of bundles of collagen and elastin

Fig. 47. Brook lampreys, Lampetra planer i.

A, ripe female, with anal fin; B, ripe male; note shape of dorsal fin and presence of

copulatory papilla. (Curves due to fixation.)

fibres, running mostly in a circular direction. This tissue is sharply
marked off from a layer of subcutaneous tissue containing blood-
vessels and fat, as well as connective tissue. There are pigment cells
in the dermis and a thick layer of them at the boundary of dermis and
subcutaneous tissue. The chromatophores are star-shaped cells whose
pigment is able to migrate, making the animal dark or pale. This
change is especially marked in the larva and is produced by variation
in the amount of a pituitary secretion (p. 107).

The head of the lamprey bears a pair of eyes and a conspicuous
round sucker. On the dorsal side is a single nasal opening, and behind
this there is a gap in the pigment layers of the skin through which the
third or pineal eye can be seen as a yellow spot. There are seven pairs
of round gill openings, which, with the true eyes (and some miscount-
ing or perhaps inclusion of the nasal papilla), are responsible for the
familiar name 'nine eyes'. There is no trace of any paired fins, but the
tail bears a median fin, which is expanded in front as a dorsal fin.
There are sex differences in the shape of the dorsal fins of mature
individuals and the female has a considerable anal fin (Fig. 47).

iv. 5

SWIMMING OF LAMPREYS

The lamprey swims with an eel-like motion, using its myotomes in
the serial manner that has been mentioned in amphioxus and will be
discussed later (p. 133). The waves that pass down the body are of
short period relative to the length, so that the swimming is mechani-
cally inefficient; lampreys show great activity, but their progress is
not rapid. The animal often comes to rest, attaching itself with the
sucker to stones (hence the name, 'suck-stone') or to its prey. In this
position water cannot of course pass in through the mouth, but both

s. cut.

Fig. 48. Section of skin of lamprey.

c. club cells; der. dermis; ep. epidermis; gr. granular gland-cells; m. myotomal muscle;
pig. pigment cells; s.cut. subcutaneous connective tissue. (After Krause.)

enters and leaves by the gill openings. When swimming the backward
jet of water may assist in locomotion.

The trunk musculature consists of a series of myotomes separated
by myocommas. Each myotome has a W-shape, instead of the simple
V of amphioxus. The muscle-fibres run longitudinally and they are
striped, but of a somewhat peculiar fenestrated type.

5. Skeleton of lampreys

The skeleton of lampreys consists of the notochord and various
collections of cartilage. This latter is partly of the typical vertebrate
type, that is to say, consists of large cells in groups, separated by a
matrix of the protein chondrin, which they secrete. In other regions
a tissue containing more cells and less matrix is found, the so-called
fibro-cartilage, and this more nearly resembles fibrous connective
tissue and serves to emphasize that no sharp line can be drawn
between these tissues. There is also, in the larva, a tissue known as

86 VERTEBRATES WITHOUT JAWS iv. 5

muco-cartilage, which is an elastic material serving more as an
antagonist to the muscles than for their attachment.

The notochord remains well developed throughout life as a rod
below the nerve-cord. It consists of a mass of large vacuolated cells,

Fig. 49. Transverse section through notochord of lamprey.
c. cells; s. sheath. (After Krause.)

anc

Fig. 50. Lateral view of skeleton of head and branchial arches of Petromyzon.

ac. auditory capsule; adc. antero-dorsal cartilage; anc. annular cartilage; ha. branchial
arch; bd. basidorsal; hac. hyoid cartilage; hbc. hypo-branchial rod; lit. horizontal bar; n.
notochord; ?ic. nasal capsule; oc. orbital cartilage; per. pericardial cartilage; pdc. postero-
dorsal cartilage; pic. posterolateral cartilage; st. styliform cartilage; /. tendon of tongue;
II-X, cranial nerves. (After Parker.)

enclosed in a thick fibrous sheath (Fig. 49). The rigidity of the whole
rod depends on the turgor of the cells and it often collapses com-
pletely in fixed and dehydrated material (Fig. 59). No doubt in life it
serves, like the notochord of amphioxus, to prevent shortening of the
body when the myotomes contract.

The notochordal sheath is continuous with a layer of connective
tissue, which also surrounds the spinal cord and joins the myocom-

iv. s SKELETON OF LAMPREYS 87

mas and thus eventually the subcutaneous connective tissue. Within
this connective tissue there develop certain irregular cartilaginous
thickenings that are of special interest because they may be compared
with vertebrae, perhaps with the basi-dorsal element (p. 132). They
lie on either side of the spinal cord (Fig. 50), that is to say, above the
notochord, and consist either of one nodule on each side of the seg-
ment, through the middle of which the
ventral nerve-root emerges, or of two
separate nodules, with the nerve between
them. Rods of cartilage extend dorsally
and ventrally into the fins, but are not
attached to the 'vertebrae'.

The lamprey skull shows even in the
adult the basic arrangement found only
in the embryo of higher vertebrates. The
floor is formed of paired parachordals on
either side of the notochord and in front
of this paired trabeculae. Attached to this
base is a series of incomplete cartilagi-
nous boxes surrounding the brain and
organs of special sense (Fig. 51). To
this skull is attached the skeleton that
supports the sucker and gills. The
arrangement of the skull differs consi-
derably from that of later vertebrates.
The cranium has a floor around the end
of the notochord, and in front of this
there is a hole containing the pituitary
gland. The side walls are strong but the roof is composed only of
a tough membranous fibro-cartilage. The auditory capsules are
compact boxes surrounding the auditory organs at the sides. The
olfactory capsule, imperfectly paired, is also almost detached from
the cranium. Other ridges of cartilage lie below the eyes and there is
a complex support for the sucker.

The skeleton of the branchial region consists of a system of vertical
plates between the gill-slits, joined by horizontal bars above and
below them. This cartilage lies outside the muscles and nerves and is
therefore difficult to compare with the branchial skeleton of higher
fishes, which lies in the wall of the pharynx. The elastic action of the
cartilages produces the movement of inspiration. A backward exten-
sion of the branchial basket forms a box surrounding the heart.

Fig. 51. Dorsal view of skull of

Petromyzon.

Lettering as Fig. 50. /, olfactory

nerve; /. hole in roof of cranium.

(After Parker.)

88 VERTEBRATES WITHOUT JAWS iv. 6

6. Alimentary canal of lampreys

The sucker is bounded at the edges by a series of lips, which besides
being sensory serve also to make a tight attachment when the lamprey
sucks (Fig. 52). In the sucker are numerous teeth, whose arrangement
varies in the different types of lamprey. These teeth are horny epi-
dermal thickenings, supported by cartilaginous pads, and are there-
fore not comparable with the teeth of vertebrates, which are derived

Fig. 52. Sucker of Petromyzon show- Fig. 53. Section through tooth of lamprey

ing outer circular lip, teeth, and tongue, 1, horny cap; 2, stellate tissue; 3, cap to replace

with special teeth, at the centre. , ; 4> connective tissue; 5, epidermis of mouth;

(After Parker.) 6, cartilage; 7, proliferative layers of epidermis

that produce the horny cells.
(After Hansen, from Kukenthal.)

mainly from mesodermal tissues (Fig. 53). The sharper and larger
teeth are borne on a movable tongue, which is used as a rasp (Fig. 54).
An annular muscle runs round just above the lips of the sucker and
presumably serves to narrow the margin and hence to release the fish.
The remaining muscles are mostly attached to the tongue and base
of the sucker. The largest of these muscles, the m. cardioapicalis, is
attached posteriorly to the cartilage surrounding the heart and in front
is prolonged into a conspicuous lingual tendon, which is attached to
the tongue and serves to pull it backwards. Presumably the action of
this muscle deepens the oral cavity and is thus the main agent securing
attachment of the sucker. There is a collar of circular fibres around
the front end of the cardio-apical muscle, serving to lock the tendon
and maintain the suction. Dorsal and ventral to the main tendon are

iv. 6

FEEDING OF LAMPREYS

groups of muscles that rock the tongue up and down to produce a
rasping action. The muscles of the sucker are all derived from the
lateral plate and are innervated from the trigeminal nerve; their fibres
are striated.

The mouth is a small opening above the tongue and leads into a
large buccal cavity. At the hind end this divides into a dorsal passage,
the oesophagus, for the food, and a ventral respiratory tube, which
leads to the gill pouches but is closed behind. At the mouth of the

ann.

m. card.ap.

circ.m.

mus.2 mus.t

Fig. 54. Longitudinal section through head of lamprey.

ann. annular muscle of sucker; b. brain; circ.m. circular fibres of tongue-muscles; oes. oeso-
phagus; g. gill aperture; h.s. hypophysial sac; m.card.ap. cardio-apical muscle; mus. 1 and
2, muscles that rock the tongue; n. notochord; nas. nasal sac; nos. nostril; p. pineal; pit.
pituitary gland; t. tooth; tend, tendon of tongue, pulled back by m.card.ap.; to. tongue. (Partly

after Tretjakoff.)

respiratory tube is a series of velar tentacles, corresponding exactly in
position to those of amphioxus, and serving to separate the mouth
and oesophagus from the respiratory tube while the lamprey is feed-
ing. The seven branchial sacs are lined by a folded respiratory epi-
thelium and surrounded by muscles, and these, together with the
elastic cartilages and appropriate valves, ensure the pumping of the
water tidally, in and out of the external openings. In front of the first
sac is the remains of an eighth pouch, whose surface is not respiratory.
The 'salivary' glands are curious organs of which little is known.
They are a pair of pigmented sacs, embedded in the hypobranchial
muscles. Each has a folded wall, from which a duct proceeds forward
to open below the tongue. The salivary glands produce a secretion
that prevents coagulation of the blood of the fishes on which the lam-
prey feeds. The nature of this secretion is not known, but it rapidly
turns black on exposure to the air and the glands for this reason
appear to be pigmented. It has been observed that in lampreys taken
from fishes the intestine is filled with red corpuscles, and there is
therefore no doubt that they feed mainly on the blood of their prey.

90 VERTEBRATES WITHOUT JAWS iv. 6-

Little is known of the habits of lampreys in the sea, but in North
America there are races of lampreys that are land-locked and feed on
the fishes in the lakes, where they have recently become a most serious
pest (Fig. 55).

The oesophagus (fore-gut) leads directly into a straight intestine
(mid-gut); there is no true stomach in lampreys (Fig. 56). The surface
of the intestine is increased by a typhlosole, running a somewhat
spiral course. There is a liver, gall-bladder, and bile-duct of typical
vertebrate plan, but no separate pancreas. However, in the wall of the

Fig. 55. Lake lamprey attached to a bony fish, which also shows the scars of the
attacks of other lampreys. (After Gage.)

anterior part of the intestine there are large patches of cells that
resemble those of the acini of the pancreas of higher forms and con-
tain secretory granules. Barrington has shown that extracts of this
region have a high proteolytic power, the enzyme being of the tryptic
type, with its optimum between pH 7-5 and 7-8. Some of this tissue is
collected in the walls of short diverticula, reaching forwards. The
situation is therefore essentially similar to that found in amphioxus,
and we may regard these patches of zymogen cells, or the diverticula,
as the forerunners of the exocrine portions of the pancreas. In the
lampreys the endocrine portion, not yet identified in amphioxus, also
appears. Around the junction of the fore-gut and intestine are groups
of follicles that do not communicate with the lumen of the intestine.
These 'follicles of Langerhans' were, appropriately enough, first seen
by the discoverer of the islets in higher forms, and Barrington has
now shown that following destruction of this tissue by cautery there
is a rise in blood-sugar. Moreover, after injection of glucose, vacuola-
tion of the cells occurs. We may safely conclude that these cells are
involved in carbohydrate metabolism, but only one type of cell is
present.

iv. 7

(9i)

7. Blood system of lampreys

The blood vascular system is arranged on the same general plan
as in amphioxus but there is a well-developed heart. This lies behind
the gills and can be considered as a portion of the sub-intestinal vessel,
folded into an S-shape and divided into three chambers. The heart
is suspended in a special portion of the coelom, the pericardium,
whose walls are supported by cartilage. In the larva the heart first
appears as a straight tube and owing to an abnormality of development
it sometimes fails to develop its S-shape. Contractions can neverthe-

Fig. 56. Mid-gut of larval lamprey.

ai. anterior region of intestine; bd. bile-duct; ca. coeliac artery; gb. gall-bladder; hp. hepatic

portal vein; /. liver; oes. oesophagus; p. position of 'pancreas', containing islet tissue;

pi. posterior intestine; y. yellow area where wall of intestine contains zymogen cells.

(From Barrington.)

less be seen in these abnormal hearts, passing from behind forwards
along the straight tube. Similarly in the normal heart contraction
proceeds in the chambers from behind forwards. The most posterior
chamber is a thin-walled sinus venosus, into which the veins pour
blood. This leads to an auricle (atrium), also thin-walled, lying above
the sinus. The atrium passes blood into the ventricle below it, a
thick-walled chamber, providing the main force for sending the blood
round the body.

The heart receives nerve-fibres from the vagus nerve and contains
nerve-cells, some of which give a chromaffin reaction suggesting the
presence of adrenalin-like substances. Stimulation of the vagus nerve
produces acceleration of the heart-beat, followed by slowing. Acetyl
choline also accelerates the heart. In Myxine there are no nerves to
the heart or nerve-cells in it and acetyl choline has no effect. Both
hearts contain much adrenaline and similar substances but show little
change when adrenaline is added to a perfusate.

Blood leaves the ventricle by a large ventral aorta, running forwards

92 VERTEBRATES WITHOUT JAWS iv. 7-

between the gill pouches, to which it sends a series of eight afferent
branchial arteries. These break up into capillaries in the gills, and
efferent branchial arteries collect to a pair of dorsal aortae, running
backwards, which join and form the main dorsal aorta. This passes
down the trunk and carries blood to all the parts of the body by means
of series of segmental arteries and special vessels to the gut, gonads,
and excretory organs. A curious feature is that many of these arteries
are provided with valves at the point at which they leave the main

trunks (Fig. 57). It may be significant
that such valves are not found where
the efferent branchials join the dorsal
aorta, nor at the points of exit of the
renal arteries, so that perhaps the
valves serve to reduce the pressure in
the majority of the arteries, while
leaving it high in those to the kidneys.
The removal of large quantities of
water is an important problem in all
freshwater animals and is facilitated
by a high pressure in the kidneys.
This must be difficult to maintain in
an animal with a branchial circulation
and hence a double set of capillaries.
The venous system consists of a
network of sinuses, with contractile
venous hearts in various places.
There is a large caudal vein, dividing
where it enters the abdomen into two posterior cardinals. These
run forward in the dorsal wall of the coelom, collecting blood from
the kidneys, gonads, &c, and opening into the heart by a single
ductus Cuvieri on the right-hand side, this being the remains of a pair
found in the larva. Anterior cardinals collect blood from the front
part of the body, and there is also a conspicuous ventral jugular vein
draining venous blood from the muscles of the sucker and gill pouches.
Besides the veins proper there is a large system of venous sinuses,
especially in the head. Blood from the gut passes by a hepatic portal
vein through a contractile portal heart to the liver, from which hepatic
veins proceed to the heart.

The blood of lampreys, like that of all vertebrates, contains the
respiratory pigment haemoglobin, enclosed in corpuscles, here nucle-
ated. This arrangement immensely increases the oxygen-carrying

Fig. 57. Valves at the origin of
segmental arteries of a lamprey.

1, notochord; 2, segmental artery; 3,

aorta.

(From Kukenthal, after Keibal.)

iv. 8 EXCRETION IN LAMPREYS 93

power of the blood. Haemopoietic tissue occurs in the intestinal wall
of the larva and this has been regarded by some as representing the
spleen. In the adult the blood-forming tissue lies below the spinal
cord and in the kidney. White corpuscles resembling lymphocytes
and polymorphonuclear cells occur, produced by lymphoid tissue in
the kidneys and elsewhere. However, there is no distinct system of
lymphatic channels.

8. Urinogenital system of lampreys

The excretory and genital systems of vertebrates consist of a series
of tubes opening from the coelom to the exterior and serving to carry
away both excretory and genital products. This plan of organization is

Fie. 58. Diagram to show arrangement of the pronephros in a freshly hatched

lamprey.
g. gonad; pr. pronephros; prd. pronephric duct. (After Wheeler.)

quite different from that found in amphioxus and represents a new
acquisition by the vertebrates. It is not clear whether the excretory
or genital component of the complex is the primary one, nor indeed
why they are associated. The gonads develop from the walls of the
coelom in all animals possessing that cavity; some hold that the coelom
represents an enlargement of a sac that at first served purely as a
gonad. Genital ducts leading from the coelom to the exterior are
common in invertebrates, and we may guess that at their first appear-
ance the urinogenital tubules of vertebrates served only for genital
products.

The conversion of these tubules to excretory purposes may have
been a result of the adoption of the freshwater habit. The blood of
lampreys, when in fresh water, contains a higher concentration of salts
than the surrounding water. Little is known about the condition in
sea lampreys, where blood is probably hypotonic to the sea. When in
the river the animals must deal with the tendency for water to flow in.
This water must be removed without losing salt ; accordingly in most
freshwater animals, including vertebrates, we find some system by
which the separation can be achieved.

94 VERTEBRATES WITHOUT JAWS iv. 8

The region that gives rise to the kidney during development lies
between the dorsal scleromyotome and the more ventral lateral plate

card v

glom

on. t

oes.

pron. F

Fig. 59. Section through newly hatched larvae of Lampetia hehind the pharynx.

ao. aorta; card.v. cardinal vein; glom. glomerulus; fit. heart; my. myotome; n.c. nerve-cord;
not. notochord, which has collapsed because of lack of turbidity after fixation; oes. oeso-
phagus; pron.f. ciliated funnel of pronephros; pron.t. twisted pronephric tubule; sp. space

around nerve-cord.

Fig. 60. Kidney system of a 22-millimetre larva of Lampetra.

tnes. mesonephric tubules; mesg!. mesonephric glomeruli; pr. pronephric funnels;
prd. pronephric duct; prgl. pronephric glomeruli. (After Wheeler.)

mesoderm; it is known as the nephrotome. This tissue differentiates
during development from in front backwards, making a series of
segmental funnels, opening into a common archinephric duct (Fig.
58). The most anterior funnels open into the pericardium; usually
there are four of these in a freshly hatched larva, opening into a single

iv. 8

EXCRETION IN LAMPREYS

mid

duct, which reaches back to an aperture near the anus. Close to each
funnel there develops a tangle of blood-vessels, the glomerulus (Figs.
59 and 6o). Presumably the osmotic flow of water into the body is
relieved by the pressure of the heart-beat forcing water out from the
glomeruli into the coelomic fluid, whence it is removed by the funnels,
with the aid of their cilia. The tubules become longer and twisted
after hatching and may perhaps serve for salt-reabsorption.

These anterior funnels constitute
the pronephros. As the animal
grows they are replaced by a more
posteror set, the mesonephros.
There is, however, a gap of
several segments in which no
tubules appear (Fig. 6o), a strange
and unexplained discontinuity,
common to all vertebrates. The
pronephric tubules gradually dis-
appear and finally in the adult all
that remains of the organ is a mass
of lymphoid tissue. Meanwhile the
mesonephros develops as a much
larger fold, hanging into the coelom
and containing very extensive wind-
ing tubules. These do not open to
the coelom (at least in the adult) but
each to a small sac, the Malpighian
corpuscle, which contains a portion
of the coelom and the glomerulus.
This is obviously a more efficient method for allowing the heart to
pump excess water out of the blood and down the tubules. The latter
themselves have become greatly elongated and make up the main
bulk of the organ (Fig. 6i). The segmental arrangement is there-
fore much obscured and as extra glomeruli are added it disappears
completely. The mesonephros extends at its hind end as the animal
grows, until it forms the adult kidney, a continuous ridge of tissue
reaching back to the hind end of the coelom. Besides the excretory
apparatus the kidney also contains much lymphoid tissue and fat, and
it probably plays a part in the formation and destruction of red and
white corpuscles.

The gonads are unpaired ridges medial to the mesonephros. Pri-
mordial germ-cells, set aside very early in development, migrate into

Fig. 6i. Transverse section of kidney of
hampetra.

gl. glomerulus; mid. middle section of

tubule; pr. proximal region of tubule; term.

terminal region, opening into W.d. Wolffian

duct.

(After Krause.)

iv. 8-

96 VERTEBRATES WITHOUT JAWS

these ridges and develop into eggs or sperms. The differentiation of
the gonad occurs relatively late in lampreys, so that in young am-
mocoetes the organ is 'hermaphrodite', containing developing oocytes
and spermatocytes together. The ripe ovary consists of ova each sur-
rounded by single-layered follicular epithelium, which finally ruptures
and liberates the egg into the coelom, whence it escapes by pores to be
described presently. The testis consists of a number of follicles con-
taining sperms; it is unique among vertebrates in that the follicles

CL U 9 .

Fig. 62. Cloacal region of fully adult Lampetra.

C. coelom; CI. lips of cloaca; Ct. connective tissue; D. duct leading from coelom to the

mesonephric duct; Df. dorsal fin; M. muscle; Md. mesonephric ducts; N. notochord;

R. rectum; Ug. urinogenital papilla. (After Knowles.)

have no ducts; when ripe they rupture into the coelom, which becomes
filled with spermatozoa and these escape, like the ova, by pores.

These apertures by which the gametes escape are similar in the
two sexes and consist of short channels, one on each side, leading from
the coelom to the lower end of the kidney duct (Fig. 62). They nor-
mally become open only a few weeks before spawning, but Knowles
has shown that injections of oestrone or anterior pituitary extract will
cause perforations of the ducts in young lampreys, indeed even in the
ammocoete larve.

Fertilization is external, but there are modifications of the cloaca in
the two sexes to assist in ensuring fertilization and proper placing of
the eggs in the 'nest' (p. 113). The lips of the cloaca of the ripe male
are united to form a narrow penis-like tube. The cloacal lips of the

iv. 9 NERVOUS SYSTEM OF LAMPREYS 97

female are enlarged and often red; in addition she has an anal fin,
probably used, as in salmon and trout, to make a nest. These sex
differences, which develop shortly before spawning, can also be
initiated by injection of anterior pituitary extracts (p. 107).

9. Nervous system of lampreys

The nervous system of the cyclostomes is very much better
developed than that of amphioxus and shows the characteristic plan
that is present in all vertebrates. The essence of the vertebrate ner-
vous organization may be said to be that it consists of large amounts
of tissue and is highly centralized. The brains of vertebrates contain
much larger aggregates of nervous tissue than are to be found in any
other animals, and this tissue produces by its actions the most charac-
teristic features of vertebrate life. Vertebrates are active, exploratory
creatures, and their behaviour is much influenced by past experience.

We shall return later to detailed discussion of the organization of
the central nervous system; now we may look briefly at the plan
found in the lamprey, as an introduction to that of other vertebrates.
As compared with amphioxus there has been a very high degree of
cephalization. The front end of the spinal cord is enlarged into a
complicated brain, and the nerves connected with a number of the
more anterior segments have become modified to form special cranial
nerves.

The spinal nerves, however, still show the plan found in amphioxus
in that the dorsal and ventral roots do not join. In amphioxus the
ventral roots contain motor-fibres for the myotomes and some
proprioceptive fibres, while the dorsal roots contain sensory fibres and
motor-fibres for the lateral plate musculature (p. 36). The details of
the composition of the nerves of lampreys are still unknown, but there
are hints of considerable deviations from this plan. The ventral roots
contain many motor fibres passing to the myotomes. The dorsal roots
consist largely of sensory fibres with bipolar cell bodies collected into
dorsal root ganglia including proprioceptor fibres from the myotomes:
it is not known whether the dorsal roots also contain any efferent
fibres. In the young larva many of the afferent fibres are the processes
of cells lying in the spinal cord (Rohon-Beard cells), which are
typical of the early stage of many chordates. There are few types
of cells in the cord at this time, allowing for only the simplest
reflex arcs.

The autonomic nervous system shows some generalized and some
special features. The gut is mainly innervated by the vagus, which

98 VERTEBRATES WITHOUT JAWS iv. 9

extends far back along the intestine. There is little contribution of
fibres from the spinal nerves to the alimentary canal, since this has no
mesentery, being attaached only at its cranial and caudal ends. There
are, however, numerous fibres from the spinal nerves to the rectum,
ureters, and cloacal region, and numerous postganglionic neurons
are found here. Nerve-cells are also found in the intestinal plexuses.

The sympathetic system consists of isolated fibres running in both
dorsal and ventral roots. Many of these run directly to their endings,
for instance in the arteries, without interpolation of neurons. A few
postganglionic cells are present, however, but they are seldom collec-
ted into ganglia. The system is therefore even more scattered than
in elasmobranchs (p. 173). The 'adrenal' system is also diffuse. There
are scattered masses of interrenal (cortical) tissue and large groups
of suprarenal (medullary) cells, especially in the walls of the veins and
the heart. The suprarenal tissue receives 'preganglionic' fibres from
the spinal nerves. Its cells sometimes seem to be connected with each
other by fibres like those of neurons and they may operate a form of
control intermediate between nervous and hormonal (Johnels, 1956).

The nerve-fibres in the nervous system of cyclostomes are not pro-
vided with myelin sheaths ; in this they resemble the nerves of amphi-
oxus. Conduction is slow in such non-medullated fibres, the only case
actually investigated in cyclostomes being the lateral line nerve of
Bdellostoma, found by Carlson to conduct at the low rate of 5 metres
a second (frog about 50 m/sec, mammals up to 100 m/sec).

The spinal cord is of a uniform transparent grey colour and is
flattened dorso-ventrally, apparently to allow access of oxygen, and
metabolites, no blood-vessels being present within the cord. How-
ever, vessels are present in Myxine in which the cord is also flat. The
nerve-cell bodies lie, as in higher vertebrates, towards the centre, but
the synaptic contacts are not made in this 'grey' matter but at the
periphery, in what would correspond to the white matter of higher
forms. The outer part of the cord is thus made up of a neuropil or
nerve feltwork, formed of the terminations of the incoming sensory
fibres and the dendrites of the motor-cells. These cells (Fig. 63) lie
in the ventral part of the cord, their axons running out to make the
large fibres of the ventral roots and their dendrites passing to all parts
of the peripheral regions of both the same and the opposite sides of the
cord. They are thus presumably able to be stimulated directly by
impulses in the processes of the afferent fibres that end in these
regions.

Direct control of the spinal cord from the brain is obtained through

(99)

neur.p.

Fig. 63. Cells of the spinal cord of the larva of Lampetra.
A „nH R We motor-cells with dendrites reaching to the opposite side; C, small cells with
^p^SSno axon; «. axon; M/. Mailer's fibres; „*«,.>. neuropil at
P periphery of spinal cord. (After Tretjakoff.)

VERTEBRATES WITHOUT JAWS

opt.L.

IV. 9

cer.

hi/pot.

Fore.
cerh. h.

Mid- Hind- brain.

opt.L med. c ^ or

Fore. - Mid- Hind- brain.

Lam.i

Fore.

Mid.

Hind — brain.

Fig. 64. Brain of the lamprey.

A, side view; B, dorsal view with choroid plexus intact; c, after removal of choroid, cereb.
cerebellum; cer. h. cerebral hemisphere; chor. choroid plexus; hypot. hypothalamus; it. iter
between third and fourth ventricles; lam.t. lamina terminalis (thickened anterior wall of
third ventricle); med. medulla oblongata; opt.L optic lobe; pin. pineal eye; thai, thalamus;
3rd v., 4th v., third and fourth ventricles. (After Sterzi.)

a number of very large Miiller's fibres, originating from giant cells in
the reticular formation of the brain, whose large dendrites (Fig. 65)
receive fibres from several higher centres, providing an uncrossed final
common pathway to the spinal cord. There is some difference of
opinion as to whether any branches of these large fibres proceed

iv. 9 BRAIN OF LAMPREYS 101

directly into the ventral roots; probably they do not do so but the
dendrites of the motor-cells branch around them and thus receive
stimulation (Fig. 63). In the earliest larva co-ordination is by a pair of
giant Mauthner cells, with dendrites among the entering fibres of the
eighth nerve and an axon descending on the opposite side. Such cells
are present in the earliest stages of nearly all fishes and amphibians.

Other nerve-cells in the more dorsal parts of the cord have no long
axons and apparently serve to connect the neuropil of the various
regions. The afferent fibres reaching the cord in the dorsal roots give
off branches that ascend for a short distance and descend for long
distances. The pathways to the brain thus pass through multiple
relays.

The brain itself (Fig. 64) is built on the typical vertebrate plan, as
an enlargement of the front end of the spinal cord, with thickenings
and evaginations corresponding to the various organs of special sense.
Although we know little of its internal functional organization in
lampreys, it is probably not far wrong to regard it as chiefly consisting
of a series of hypertrophied special sensory centres; thus the forebrain
is connected with smell, midbrain with sight, hind-brain with
acoustico-lateral and taste-bud systems. The forebrain and olfactory
sense are moderately well developed in adult lampreys, as is the visual
sense, with its chief centre in the midbrain. The auditory and acoustico-
lateral systems are not very well marked, and the cerebellum is small.
Taste is also much less developed than in the higher fishes (p. 220).

Parts of the brain

Forebrain (prosencephalon) Cerebral hemispheres (telen-

cephalon)
Between-brain (diencephalon)
Midbrain (mesencephalon) Optic lobes

Hind-brain (rhombencephalon) Cerebellum (metencephalon)

Medulla oblongata (myelen-
cephalon)

The upper surface of the brain is covered by an extensive vascular
pad, the choroid plexus or tela choroidea (Fig. 64). This extends into
the ventricles of the brain at three points — into the third ventricle of
the diencephalon, into the iter (duct) leading through the midbrain
from third to fourth ventricles, and into the fourth ventricle itself.
The roof of the brain is thus non-nervous in these regions. In later
vertebrates the choroid extends only into the third and fourth

io2 VERTEBRATES WITHOUT JAWS iv. 9-

ventricles. Presumably the vascular membranes of the brain are highly
developed in lampreys because of the absence of cerebral blood
vessels.

From the lower part of the mid- and hind-brain arise all the cranial
nerves except the olfactory and optic. These nerves follow the same
plan as those of gnathostomes but they are difficult to make out by
dissection in the lamprey and will be left for consideration in con-
nexion with the dogfish, in which they can easily be dissected. The

beet. opt.
chor. pL3

chor.pt, 4.

otf.ep — IM-<^9 %

/nterped.

Fie. 65. Sagittal section through head of lamprey.

cereb. cerebellum; cer.h. cerebral hemisphere; chor.pl. 3 & 4, choroid plexuses of the 3rd and
4th ventricle, extending also into the midbrain; h.s. naso-hypophysial tube; hab. habenular
region; hyp. hypothalamus; interped. interpeduncular region; med. medulla oblongata; Mull.
M Oiler's cell; not. notochord; o. glandular organ of nasal sac; olf.ep. olfactory epithelium;
olf.n. olfactory nerve; p. ant., p. int., and p.nerv. partes anterior, intermedia, and nervosa of the
pituitary gland; parap. parapineal; pin. pineal; ted. opt. tectum opticum.

cranial nerves represent nerves similar to the dorsal and ventral nerve-
roots of the trunk, much modified as a result of the special develop-
ment of the head (p. 148). They carry afferent fibres from the skin of
the head and gills and motor-fibres for moving the eyes, sucker, and
branchial apparatus.

From the relative sizes of the parts of the brain it can be seen that
the various special sensory centres are still small. The largest part of
the brain is the medulla oblongata, which is well developed because

iv. io PINEAL EYES OF LAMPREYS 103

of the extensive sucking apparatus, innervated from the trigeminal
nerve.

The forebrain consists of a pair of large cerebral hemispheres and
these open by the foramina of Munro into a median third ventricle,
whose walls constitute the diencephalon or between-brain (Fig. 65).
This diencephalon, besides connecting the forebrain with the mid-
brain, includes the thalamus and serves important functions of its own.
Its ventral part, the hypothalamus, is well developed in all vertebrates
as a central organ controlling visceral activities and the internal life
of the organism. Nerve-fibres from the supraoptic nucleus of the
hypothalamus proceed to the pars nervosa of the pituitary and, as in
other vertebrates, are filled with granules of neurosecretory material,
which presumably controls pituitary action. A simple portal system
of blood-vessels connects the hypothalamus with the pituitary.

10. The pineal eyes

The diencephalon is also the region of the brain from which the
eyes are formed. In lampreys, besides the usual pair of eyes, there is
also, attached to the roof of the between-brain, the so-called third,
epiphysial, or median eye, better developed in these animals than in
any other living vertebrate except perhaps certain reptiles.

This organ is actually not median but consists of an unequally
developed pair of sacs, that on the right, the pineal, being larger and
placed dorsal to the morphologically left parapineal (Fig. 66). The
sacs form by evagination from the brain and remain connected with
the dorsal epithalamic or habenular region of the between-brain by
two stalks. The two organs are similar in structure, consisting of
irregular flattened sacs with a narrow lumen. Both upper and lower
walls of each organ contain receptor cells, with processes that project
into the lumen and nerve-fibres directed outwards. These fibres
apparently mostly end within the organ, in contact with ganglion
cells whose axons run to unequal right and left habenular ganglia.
In addition there are supporting and pigment cells in the retinas.
Knowles has shown that the retinal cells of the pineal make movements,
being arranged differently under conditions of illumination and dark-
ness. The significance of these photomechanical changes is unknown
but they demonstrate that the pineal cells are sensitive to light.

The structure of these pineal organs shows that they consist of
portions of the diencephalic wall where the ciliated cells of the epen-
dyma are specialized as photoreceptors. They show the same general
plan as the paired eyes, but with no differentiated dioptric apparatus.

IV. IO

104 VERTEBRATES WITHOUT JAWS

It has been possible to find out something of the part that these
organs play in the life of the lamprey. When a bright spot of light is
directed upon the pineal region of a stationary ammocoete larva move-
ment is usually initiated, but only after illumination for many seconds.

o.s.s.

Fig.

t.s.s., o.s.s

66. Pineal and parapineal organs of adult Lampetra fluviatilis
A. larva, B. adult. Sagittal section.

, inner and outer sensory cells; p. process; pin. pineal; p. pin. parapineal.
(After Tretjakoff.)

Moreover, these movements can be elicited even after the pineal
organs have been removed! In the larval lamprey the paired eyes are
deeply buried below pigmented skin, so the movement is not likely
to be due to them; indeed it continues when they too have been taken
out! Evidently there must be still other receptors, able to respond to
changes of light intensity in the wall of the diencephalon. This recalls
the fact that photoreceptors are found within the substance of the
nervous system of amphioxus. This power of response to changes of
illumination has been retained in the vertebrates, and persists in some

FUNCTION OF PINEAL EYES

105

as yet unknown cells in the brain, even after the paired and pineal
eyes have become specialized for light reception. The whole study is
of special interest as showing the stages by which the eyes may have
been evolved. Higher fishes also show the power of responding to

PINEALS REMOVED
1

rm — 1 1 1 1 1 1 1 1 1 1 M 15.

I I I i I I I I 1 ! ! I I I I II 1 I I II I I

\t up

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15 20 25 30 I S

I I M I I I I I I I I I I I I I I I I I I I I I I

DECEMBER JANUARY

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MARCH

Fig. 67. Colour-changes of larval lampreys, measured by the melanophore index (see
p. 300). Animals kept out of doors except as shown along the line AB, where rect-
angles above the line show illumination with electric light and below the line total
darkness. Normal animals show a regular daily rhythm, becoming pale at night.
Reversal of normal day and night illumination stops the change. On 19 December
the pineal eyes were removed from five out of the ten individuals and these there-
after remained dark (upper chart); the other five continued to show the normal
rhythm, until placed in total darkness. (After Young.)

changes of illumination after the paired eyes and epiphysis have been
removed (p. 210).

If the pineal eyes are not essential for the initiation of movement,
what is then their function ? In the ammocoete larva there is a daily
rhythm of change of colour, the animals becoming dark in the day-
time and pale at night. After removal of the pineal eyes this change no
longer occurs: the animals remain continually dark (Fig. 67). This
effect on the colour is produced by the action of influences from the
pineal, passing to the pituitary gland (see p. 103). It seems that
the pineal apparatus is an organ concerned with adjustment of the
internal activities of the animal to correspond to the changing con-
ditions of illumination. The control may be effected by impulses

io6

VERTEBRATES WITHOUT JAWS

carried in the large tract that proceeds from the habenular ganglion
to the hypothalamus, in the floor of the diencephalon. The latter is
known to be concerned, throughout the vertebrate series, with the
integration of the internal activities of the animal.

¥ d Y

pner.

p. int.

pant

Fig. 68. Sagittal section of the pituitary gland of lamprey.

dien. diencephalon; inf. infundibulum; p.ant., p.int., and p. tier, partes anterior, intermedia,

and nervosa, there are two types of cell in the pars anterior; 3rd V. third ventricle.

(After Stendell.)

3 4 5 6

Hours after operation

FlG. 69. Onset of pallor in a larval lamprey after removal of the pituitary gland,
as shown by the decline in the melanophore index. (From Young.)

1 1 . Pituitary body and hypophysial sac

The lower portion of the diencephalon, the hypothalamus, forms
a prominent pair of sacs, the lobi inferiores, which contain a partly
separated diverticulum of the third ventricle and end below in the
infundibulum (Fig. 65). The pituitary gland (hypophysis) is pressed
against the underside of the hypothalamus (Fig. 68). The lower wall
of the brain in this region consists not of nerve-cells but of a single

IV. II

PITUITARY OF LAMPREYS

107

-^fMvn/w^^

epithelial layer, corresponding to the pars nervosa of the pituitary of
higher forms. The major portion of the pituitary gland is a mass of
secreting cells in which two parts can be recognized, the partes
anterior and intermedia. After experimental removal of the inter-
mediate portion of the pituitary lam-
preys become permanently pale in
colour (Fig. 69), showing that, as in
other vertebrates (p. 299), a melano-
phore-expanding substance is liberated
into the blood by this gland, the secre-
tion being presumably under the control
of the pineal eyes (p. 105). The lamprey
pituitary has been shown to contain
oxytocic and 'water balance' hormones
as well as one producing melanophore
expansion. Moreover injections of
mammalian anterior pituitary extracts
induce appearance of the secondary
sexual characters of lampreys. Evi-
dently the functions of the pituitary
have remained essentially the same
through the whole chordate series.

The pituitary of lampreys is peculiar
because of great development of the
naso-hypophysial sac (Fig. 70). Charac-
teristically in vertebrates the pituitary
body develops by the formation of a
pocket of buccal ectoderm, whose walls
then become folded, so that the part
in front of the lumen becomes the pars
anterior, that behind the pars inter-
media. In nearly all vertebrates the
lumen then loses its connexion with the
exterior. In lampreys the hypophysial
rudiment is continuous with that of the
olfactory epithelium. The latter then
moves dorsally and the two remain

connected throughout larval life by a strand of cells. At metamorphosis
this acquires a lumen and forms a tube extending from the nostril
below the pituitary and brain. Because of its development this is
sometimes called the naso-hypophysial tube but others doubt that

Fig. 70. Dissection of lamprey from
the ventral surface after injection
of coloured gelatine to show the
outline of the naso-hypophysial sac
(.1) and its duct (d), which is shown
dotted where it runs upwards be-
tween the nasal sacs («). g, gill
pouches. Contraction of the bran-
chial apparatus squeezes the sac s,
so that water is drawn in at each
relaxation.

io8

VERTEBRATES WITHOUT JAWS

IV. II-

it represents the cavity of the hypophysis and prefer the name
nasopalatine canal.

Inside the single nostril, guarded by a valve, are openings into the
nasal sacs, which are cavities with folded walls. Some of the cells of
these walls are the olfactory receptors and give off the axons that make
up the olfactory nerves, entering the olfactory bulbs on the anterior
end of the hemisphere (Fig. 65). Behind the nasal sacs lie numerous
glandular follicles opening into the sac in the larva, but completely
closed in the adult (Fig. 65). They may be comparable to Jacobson's
organ (p. 405).

Fig. 71. Section of lateral line organ of tail of adult Lampetra.

p. pigmented cells around the pit; s.c. receptor cells
(not showing long hairs). (After Young.)

The naso-hypophysial tube proceeds back behind the pituitary to
a closed sac lying between the first pair of gill pouches (Fig. 70).
During the movements of respiration this sac is squeezed and water
is expelled with some force through the nostril. When the gills relax
water flows in at the nostril, and in this way the olfactory organ is
provided with samples. If the naso-hypophysial opening is closed with
a plug of plasticine the lamprey no longer reacts to solutions, for
instance of alcohol, to which it normally responds by freeing its
sucker and swimming away.

12. Lateral line organs of lampreys

The lateral line receptors, peculiar to fish-like vertebrates, are little
patches of sensory cells found along certain lines on the head and
trunk. They are all innervated by cranial nerves, those on the body
and tail being served by a special backward branch of the vagus nerve.
The receptor cells carry long hairs and are thus able to detect either
movement of the water relative to the fish or of the fish itself. Objects
moving nearby set up disturbances that may also be detected (p. 218).

v. i3

LABYRINTH OF LAMPREYS

109

In the lamprey the lateral line organs are very simple (Fig. 71), being
open to the exterior and not sunk in a canal as in higher forms. The
rows are somewhat irregular, especially those on the body.

13. Vestibular organs of lampreys

The labyrinth may be considered as a specialized portion of the
lateral line system, concerned with recording the position of the head

end.

mac.laq. \ mac.ut.
3 mac. sac.

smp.p.

amp a.

Fig. 72. Labyrinth of right side, seen in lateral view. A and B,

Lampetrci, c, Myxitie.

a.c. anterior canal; amp. a. and p. anterior and posterior ampullae; cil.

ciliated chamber; cr.a. and p. cristae; end. endolymphatic duct; lag.

lagena; mac. lag., neg., sacc, ut. maculae of the lagena, neglecta,

saccule, and utricle; p.c. posterior canal. (After de Burlet.)

and angular accelerations. There is no evidence to decide whether
lampreys can respond to sound. The labyrinth develops by an in-
pushing of the wall of the head, and this then becomes closed off from
the exterior. Internal foldings divide up the sac into a number of
chambers, which differ considerably from those of gnathostomes.
There is a large central vestibule, into which open below several
partially separate sacs, provided with patches of sensory hairs. These
correspond, from in front backwards, to the maculae of the utricle,
saccule, and lagena of higher forms (Fig. 72). The hairs of the maculae
are loaded with otoliths. There are only two broad semicircular
canals, corresponding to the anterior and posterior vertical canals
of other vertebrates, each with an ampulla, containing a receptor
ridge, the crista. Also opening to the vestibule are two large sacs,

no VERTEBRATES WITHOUT JAWS iv. 13-

covered with cilia (Fig. 72), whose beat produces complicated
counter currents in the dorso-ventral plane. It has been suggested
that these function as a gyroscope, compensating for the absence of
a horizontal canal.

In Myxine the condition is even simpler, there being only a single
vertical semicircular canal (Fig. 72). However, it is claimed that this

Fig. 73. Horizontal section of the eye of a lamprey.

er., ir., sr., external, internal, and superior rectus muscles; v.v. venous sinuses which cushion
the eye. (From Walls, The Vertebrate Eye, Cranbrook Institute of Science.)

has cristae at both ends. The macular system also does not show the
characteristic subdivisions but is a single macula communis.

14. Paired eyes of lampreys

The structure of the paired eyes is similar to that in other verte-
brates. They are formed, like the pineal eyes, by evaginations of the
wall of the diencephalon; the so-called optic nerve is therefore not
really a peripheral nerve but a portion of the brain; it should strictly
be called the optic tract. The eyes are moved by extrinsic muscles
arranged in a somewhat unusual manner. Accommodation is effected
by a process found in no other vertebrates. The cornea consists of two
distinct layers, separated by a gelatinous substance. Attached to the
outer (or dermoid) cornea is a cornealis muscle, apparently of myo-
tomal origin, which flattens the cornea and pushes the lens closer
to the retina (Fig. 73). There is an iris, outlining a round pupil, which
changes little, if at all, in diameter under different illuminations. Most
species of lampreys are diurnal animals. They are said to move towards

iv. is

PHOTORECEPTORS OF LAMPREYS

white objects and probably use both the eyes and the nose to find
their prey. In the ammocoete larva the paired eyes are buried below
the pigmented skin and the animal makes no movements when light
is shone on to this region.

The optic tracts of adult lampreys end in the roof of the midbrain
(tectum opticum) which is a highly differentiated, stratified region.
Besides the optic fibres it receives also impulses from fibres ascending
from the spinal cord and others from the auditory and lateral line

Fig. 74. Experiment to show behaviour of larval lampreys when illuminated. The
tank is left in total darkness and the larvae settle in all parts. When the light is
switched on those in the illuminated part begin to swim and continue to do so until
by chance they arrive in the darkened part, where they settle down. (From Young.)

centres. The midbrain is therefore undoubtedly one of the most
important parts of the brain in lampreys, though nothing is known in
detail of its functions. Its cells control movements of the animal, by
means of fibres that run to make connexion with the dendrites of the
large Midler's cells, whose axons pass down the spinal cord; other
fibres from the tectum opticum reach to various parts of the brain,
and it is probable that its activities are closely correlated with those of
many other regions.

15. Skin photoreceptors

Like many lower vertebrates the lamprey has light-sensitive cells in
the skin, as well as those in the eyes. These receptors are abundant in
the tail and if a light is shone on to this region the animal rapidly
moves away (Figs. 74 and 76). If the spinal cord is cut just behind the
head and a light then shone on to the tail, the head will be seen to
move. This suggests that the impulses are carried forwards by means
of the lateral line nerves, which is confirmed by the fact that if these
latter are sectioned, leaving the spinal cord intact, then no movements
follow when the tail is illuminated. This sensitivity of the lateral line

ii2 VERTEBRATES WITHOUT JAWS iv. 15-

organs to light is not found in other fish-like vertebrates. Indeed the
receptors are not strictly lateral line organs but pigmented epidermal
cells. The sensitivity curve shows a sharp peak at 530 m/x, this being
the region of the spectrum at which light penetrates farthest into sea
water. The pigment is probably a porphyropsin (Steven, 1950).

In hag-fishes (Myxine) the head and cloacal regions are more
sensitive to light than is the rest of the body. The impulses from the
skin are conducted through the spinal nerves in these animals, not
the lateral line nerves.

16. Habits and life-history of lampreys

We have very little information about the life of lampreys during
the time that they are in the sea. They are caught in considerable
number attached to other fishes. It is not known how many years a
lamprey spends in the sea, but it returns only once to the river for
spawning and dies after this act. The up-river migration of L. fluvi-
atilis occurs in the autumn, for instance large numbers come up the
River Severn and are caught in traps on the way, for use as food. The
spawning migrations of lampreys may take them for hundreds of
miles, for example, those of the eastern Pacific ascend to the head-
waters of the Columbia River. They are said to perform remarkable
feats of climbing, leaping from stone to stone and hanging on by their
suckers. During this period of migration some lampreys assume
brilliant orange and black colour patterns. On the other hand, lam-
preys land-locked in the lakes of New York (Petromyzon marinus
unicolor) feed in fresh water and ascend only a few miles up streams
to breed.

Once in the river the lampreys do not feed again but live over the
winter on the reserves accumulated in the form of fat, especially under
the skin and in the muscles. During the winter the gonads ripen pro-
gressively and the secondary sexual characters begin to become appar-
ent only in February. The females then develop a large anal fin, while
in the male a penis-like organ appears (Fig. 47) and the base of the
dorsal fin becomes thickened.

Spawning occurs in the spring and is preceded by a form of nest-
building. Numerous lampreys collect together, usually at a place
below a weir where the water is shallow and rather swift, and the
bottom both stony and sandy. Stones are then dragged by the mouth
in such a way as to make a small depression. Fertilization is secured
by a process of copulation in which the male fixes by the sucker on to
the fore-part of the female and the two then become intertwined and

iv. 1 6

REPRODUCTION OF LAMPREYS

undergo rapid contortions, the eggs being squeezed into the water,
while sperms are ejected through the 'penis' (Fig. 75). Fertilization
is therefore external, but the sperms must be placed very close to the

Fig. 75. Spawning lampreys seen in their nest.
(After Gage.)

eggs, for they remain active only for about one minute after entering
the fresh water, which provides the stimulus that activates them. The
eggs and sperms are not all laid at once; mating is repeated several
times until all the products have been shed, after which the animals
are exhausted and soon die. The movements of the animals stir up
the sand in the nest (this is probably the function of the anal fin of
the female) ensuring that the eggs are covered up as they are carried
away by the current.

ii 4 VERTEBRATES WITHOUT JAWS iv. 17

17. The ammocoete larva

The eggs contain a considerable quantity of yolk, but their cleavage
is total and proceeds in a manner not unlike that of the frog. After
about three weeks the young hatches as the ammocoete larva, about
7 mm long. At first this is a tiny transparent creature, but its larval
life lasts for a long time, during which it grows into an opaque eel-like
fish, up to 170 mm long (Fig. 76).

Fig. 76. Ammocoete larva of Lampetra planeri, showing the effect of shining a narrow

beam of light on to various parts of the side of the body. Illumination of 1, 2, or 8 is

followed by movement after a few seconds, but no movement follows illumination at

points 3-7. (From Young.)

end.

Fig. 77. Young ammocoete larva of lamprey fixed while feeding on green flagellates
and detritus and then stained and cleared.

an. auditory sac; br. brain (covered by meninges); e. eye; end. endostyle \f.c. food cord in
pharynx; h. heart; /. liver; m. mid-gut; oes. oesophagus; v. velar fold.

This portion of life is spent buried in the mud, the animals emerg-
ing only occasionally to change their feeding-ground, presumably if
the mud is not sufficiently nutritious. There is no sucker, the mouth
being surrounded by an oral hood rather like that of amphioxus (Fig.
77). The paired eyes are covered by muscles and skin. The head at
this stage is little sensitive to light, but the animal quickly begins to
swim if the tail is illuminated. We have seen already (p. 108) that in
lampreys there are photoreceptors in the tail, connected with the
lateral line nerves. In the larva these are the main photoreceptors, and
they ensure that the animal lies completely buried.

If a number of larvae are left in a vessel with a layer of mud on the

iv. i7

AMMOCOETE LARVA
r 2 3

Fig. 78. Development of the endostyle of the lamprey. Sagittal sections through

the head at three stages.

1, auditory sac; 2, medullary tube; 3, myotome; 4, conus arteriosus; 5, endostyle; 6, first

gill-slit; 7, first arterial arch; 8, notochord; 9, inpushings which cut off the endostyle from

the pharynx; 10, aorta; 11, stomodaeum. (After Dohrn, from Kukenthal.)

bottom they rapidly disappear and remain hidden indefinitely, the
heads perhaps just visible in small depressions made by the rhythmic
respiratory movements. When disturbed they always swim with the
head downwards and in contact when possible with the ground. This
habit leads them to burrow rapidly. It is not known whether they
have other receptors to guide them to mud rich in possible food
organisms. The nasal and hypophysial sacs are poorly developed in the
larva, and the sense of smell can hardly serve this purpose.

(n6)

t.m

bEd.

Fig. 79. A, Transverse section of endostyle of ammocoete larva.

cav. cavity of the gland; cil.g. ciliated groove in floor of pharynx; lam. lamellae of gills;
ph. cavity of pharynx; seer, mucus-secreting cells of the gland.

b, Transverse section of thyroid follicles of adult. (After Young and Bellerby.)

C, Cross section of endostyle of ammocoetes larva of Petromyzon tnarinus at level
where it is connected by a duct to the pharynx. Autoradiograph showing distribu-
tion of protein-bound I 131 . The radioactive clumps of cellular debris in the
glandular lumen and in the duct suggest that the material represents a holocrine
secretion, which will probably be absorbed in the intestine.

d. duct; hs. cellular debris; ph. pharynx; t II d. type II dorsal cells;
t III epithelial cells,

iv. 17 FEEDING OF AMMOCOETE LARVA 117

Feeding takes place by the intake of water through the mouth and
the separation of small food particles from it in the pharynx (Fig. 77).
For this purpose there is used a great quantity of mucus, which is
secreted by the endostyle and gathered into a strand by the cilia of
the pharynx. This endostyle is a most remarkable organ, forming early
in development as a sac below the pharynx (Fig. 78). It consists of a
pair of tubes, on the floor of which there are four rows of secretory
cells (Fig. 79). There is a single opening to the pharynx, by a slit
at about the middle of the length. As development proceeds the inner
rows of cells at the hind part of the organ become coiled upwards, and
at the end of larval life the endostyle therefore forms a very large mass
below the pharynx, composed of tubes lined partly by secretory and
partly by ciliated cells. Probably no enzymes are secreted by the
endostyle, its function being to produce mucus in which the food
particles become entangled. Although it resembles the endostyle of
amphioxus in the arrangement of the secretory columns, there is a
difference in that the organ in the ammocoete larva is not an open
groove. There is, however, a ciliated groove in the floor of the pharynx,
that is to say, on the roof of the endostyle (Fig. 79).

The details of the feeding-currents of the ammocoete larva are not
understood. An important difference from the arrangement in am-
phioxus is that the current is produced by muscular rather than ciliary
action. The velum, a pair of muscular flaps, provides the main current
when the animal is at rest. The branchial basket can also be expanded
and contracted by an elaborate system of muscles. It is not easy to
observe how the food particles are taken up from the current, but
apparently a strand of mucus shoots from the endostyle and occupies
the whole of the centre of the pharynx (Fig. 77). This strand probably
rotates and as it passes backwards into the eosophagus it catches the
particles.

Evidently the system enables the animals to feed efficiently on the
small unicellular algae and bacteria of the mud. In amphioxus the
ciliated pharynx, occupying a considerable proportion of the whole
surface, is only able to support a tiny creature, but the muscular
feeding-system of the ammocoete allows a relatively small pharynx to
feed a fish 170 mm long and weighing up to 10 grams. This use of
muscles for moving the gills was evidently an important step in
chordate evolution. It allowed the animals to escape from the limita-
tion of size imposed by the ciliary method of feeding. After the
development of jaws to form a still more efficient feeding mechanism
the rhythmic movement of the branchial apparatus persisted for the

n8 VERTEBRATES WITHOUT JAWS iv. 17-

purpose of respiration. We cannot be certain about changes which
occurred so long ago, but it seems likely that the respiratory move-
ments of a fish were first introduced to provide food rather than
oxygen.

The endostyle therefore shows the survival of the primitive feeding-
methods of chordates, but it also undergoes at metamorphosis an
astonishing change into a thyroid gland. The mucus-secreting columns
shrink and the whole organ becomes reduced to a row of closed sacs,
lying below the pharynx (Fig. 79 b). Each of these sacs is lined by an
epithelium, contains a structureless 'colloid' substance, and is there-
fore closely similar to a thyroid vesicle. Moreover, experiments have
shown that extracts of this organ contain iodine and exert an accelerat-
ing effect on the metamorphosis of frog tadpoles. Although nothing is
known of the part played by the secretion of this gland in the life of
the adult lamprey, we may safely conclude that we have here the
conversion of an externally secreting feeding-organ into a gland, of
internal secretion. The actual mucus-secreting cells are not trans-
formed into those of the thyroid follicles, these latter are derived from
epithelial cells in the wall of the larval organ. One cannot avoid specu-
lating on this extraordinary change of function. It may perhaps be
significant that the endocrine gland that regulates basal metabolism
(the thyroid) is derived from the part of the feeding-system that in
the earliest chordates was responsible for providing the raw materials
of metabolism. Experiments with radioactive iodine show that this
element is concentrated in certain cells of the larval endostyle (Fig.
79 c). Moreover, after addition of the anti-thyroid substance thiourea
to the water there are changes in the endostyle. Thyroxine has been
extracted from the gland and it probably has an endocrine function
as well as secreting mucus, though no one has ever produced any
changes in larval lampreys by administering thyroid hormones.
Lampreys thus show, as larvae, a stage in which the accumulation of
iodoproteins, previously widespread, becomes concentrated in the
pharynx. Perhaps at this site there were already cells specialized for
halide transport (cf. the chloride-secreting cells of teleosts, used for
osmogulation, p. 203). In adult lampreys and all higher chordates the
iodoprotein is secreted into the blood under the control of blood-
borne signals (Fig. 80). The change may well be related to develop-
ments in the regulation of metabolism, which, in the animals with a
fully endocrine thyroid becomes more nearly independent of varia-
tions in the external supply of iodine.

The great change in the endostyle is only part of the complete

RACES OF LAMPREYS

119

metamorphosis by which the ammocoete larva changes into an adult
lamprey. The mouth becomes rounded and its teeth, tongue, and
complex musculature develop. The paired eyes (previously buried)
appear; the olfactory organ becomes internally folded, and the olfac-
tory nerve and tracts much enlarged. The naso-hypophysial sac grows
backwards to the gills. In the pharynx the gills develop into sacs
opening to the branchial chamber. Changes also take place in the

Fig. 80. Diagram to show distribution of iodoproteins, at first in exoskelctal struc-
tures, as in many invertebrates and in tunicates (a). Some of this material is
concentrated in the pharynx. This tendency is exaggerated in amphioxus and the
ammocoete larva, and in the adult lamprey and later animals this pharyngeal
material forms the thyroid. A. Many invertebrates and tunicates ; n. Amphioxus ;
c. Ammocoetes; D. Metamorphosis of ammocoetes; e. General vertebrate type.
(After Gorbmann, A., in Comparative Endocrinology. Wiley, New York.)

intestine. The yellow-brown colour of the larva gives place to the
black with silver underside of the adult. The animal more and more
frequently leaves the mud and finally migrates to the sea to begin its
parasitic life.

18. Races of lampreys, a problem in systematics

Besides the river lampreys, such as L. fliwiatilis (Linn.), which
show this characteristic migratory life-history, there are also in various
parts of the northern hemisphere small brook lampreys ('prides'),
such as L. planeri Bloch, which remain throughout their life in fresh
water. These prides are very abundant in many English rivers and
streams, but since the greater part of their life is passed in the am-
mocoete stage they are not often seen. The larvae remain in the mud

izo VERTEBRATES WITHOUT JAWS iv. 18

probably for three years and undergo metamorphosis in late summer
and autumn. The characteristic of this type of lamprey is that the
adults never migrate and never feed. The gonads are already well
developed at metamorphosis and ripen during the winter. Spawning
takes place in March or April and the animals then die.

There has been much dispute about the status of these freshwater
races. In structure the adult L. planeri is nearly if not quite identical
with an adult L.fiuviatilis, except that the latter is much the larger and
has sharper teeth. Crossing of the two sorts could presumably never
take place in nature, on account of the size difference, but by artificial
stripping of the adults cross-fertilization in both directions can easily
be achieved. Unfortunately the hybrid larvae have never been reared
to maturity; we cannot therefore say whether the small size and
failure to migrate of the planeri forms are inherited characters or
are produced by the influence of the environment. The effect of the
non-migratory condition is to enable the lampreys to colonize very
fully rivers that, because of effluents, they would be unable to occupy
if a migration to the sea was necessary. By this process of acceleration
of the development of the gonads a dangerous stage in the life-history
has been avoided.

Similar pairs of migratory and non-migratory forms of lamprey are
found in Japan and in North America. Indeed, the condition appears
to be developing independently in several river systems in the United
States. Since it may be difficult for the brook lampreys to spread
from one river system to another it is possible that many of the
planeri forms have evolved separately, perhaps quite recently. If so,
this is a remarkable example of a similar response produced in different
parts of a population by a similar environmental stimulus, in this
case the effluents. This process of alteration in the relative times of
metamorphosis and sexual maturity (paedomorphosis) has occurred
also in certain amphibians (the axolotl) and in tunicates (Larvacea).
Similar changes in rates of development may have been essential
factors in the development of the whole chordate phylum (p. 77).

In one race, found in Italy, ammocoetes with mature gonads have
been reported. However, in most of these lampreys the paedomor-
phosis is only partial : metamorphosis does take place, but is immedi-
ately followed by maturity. Since in mammals injections of anterior
pituitary extracts accelerate development of the gonads, it was thought
possible that complete neoteny might be produced by making such
injections into larvae of L. planeri. No completely sexually mature
ammocoetes have yet been produced by this method, but following

iv. 18 NOMENCLATURE FOR LAMPREYS 121

the injections the larvae assumed the secondary sexual characters,
which are normally shown only at maturity, namely, swelling of the
cloaca, opening of the pore from coelom to exterior, and the changes
in body form. No signs of metamorphosis were produced by these
injections and we are left without information as to the cause of that
change in the lamprey. In Amphibia even very young larvae undergo
metamorphosis when treated with thyroid extracts, but similar treat-
ment of ammocoete larvae has failed to produce any change. Further
investigation of the problem should be very interesting, since it seems
likely that the differences between the fluviatilis and planeri forms are
the result of an endocrine factor accelerating the onset of sexual
maturity in the latter. The fact that the change is occurring in various
parts of the world adds further interest to this example of evolution
in progress.

Besides all these relatively small lampreys, there is a much larger
form, the sea lamprey, Petromyzon marinns Linn., reaching to over a
metre in length. This animal differs from Lampetra in body form,
structure of sucker, and other features, as well as in size. Like most
other groups of animals lampreys therefore present several problems
of nomenclature. Linnaeus included the three types that occur in
Europe in the one genus Petromyzon ; since they are all rather alike in
shape this is in some ways a reasonable procedure. But are we then
also to include in the same genus forms that differ more widely, such
as those occurring in the southern hemisphere ? As so often happens,
systematists have chosen the course of splitting up the Linnaean
genus, even though several of the resulting genera have only one
species. Thus Gray suggested the genus Lampetra for the brook and
river lampreys, keeping Petromyzon for the larger species of sea
lamprey. Other genera have been added, such as Entosphenus Gill for
some of the North American forms and Mordacia Gray and Geotria
Gray for the forms from the southern hemisphere (Chile, Australia,
and New Zealand). Such distinctions, though they may seem irritating
at first sight, are an advantage in that they call attention to the differ-
ences which exist. For instance, it is a striking fact that lampreys are
found in temperate waters of both hemispheres, but not in the tropics,
and it is interesting to learn that the forms from New Zealand,
Australia, and South America (there are none in South Africa) show
distinct peculiarities. Thus Geotria possesses a large sac behind the
sucker.

A special problem of nomenclature arises from the fact that the
river and brook lampreys are almost identical in structure and differ

i22 VERTEBRATES WITHOUT JAWS iv. 18-

mainly in size, time of sexual maturity, and habits. A further com-
plication is that the germ-cells of the two races allow cross-fertiliza-
tion, although this probably never occurs in nature! We may take
Dobhzansky's definition of species as 'groups of populations which
are reproductively isolated to the extent that the exchange of genes
between them is absent or so slow that the genetic differences are not

Fig. 8i. Myxine, partly dissected.

i, cloaca; 2, testis; 3 and 4, ovary with eggs; 5, liver; 6, branchial opening; 7, mouth;
8, nostril; 9 and 11, slime glands; 10, intestine. (After Retzius, from Kukenthal.)

diminished or swamped', and in this sense we may retain the specific
names L. fluviatilis and L. planeri for the two populations.

19. Hag-fishes, order Myxinoidea

The hag-fishes, Myxine and Bdellostoma (Fig. 8 1 ), are animals highly
modified for sucking. They live buried in mud or sand and probably eat
polychaetes and other invertebrates, as well as scavenging dead fishes.
The eyes are functionless rudiments, though the animals are sensitive
to changes of illumination, through skin receptors. There are sensory
tentacles around the mouth, and in both hag-fishes the teeth and
sucking apparatus are well developed. They burrow into the bodies
of dead or dying fishes. As many as 123 Myxine have been taken from
a single fish. Since the introduction of trawling they have become less
common in the North Sea, where they used to be a serious source of
loss to fishermen by their attacks on fishes caught in drift nets or on
lines. They seem to find fish when they are dying or just dead, and
entering by the mouth of their prey eat out the whole contents of the
body, leaving a sack of skin and bones. When they are themselves

IV. 19

HAG-FISHES

123

caught on lines (for instance, with a salted herring bait) the hook is
swallowed so deeply that it may be found near the anus!

The gills are modified into pouches (6-14 in Bdellostoma, 6 in

-5

Fig. 82. Arrangement of gills in Bdellostoma and Myxine.

1, tentacles; 2, wall of pharynx ; 3, branchial sac opened to show gill lamellae; 4, branchial

duct; 5, branchial sac; 6, mouth; 7, common branchial aperture in Myxine.

(From Kukenthal after Dean.)

Myxine), opening by tubes into the pharynx, and to the exterior (Fig.
82). In Myxine all the tubes are joined and open by a single posterior
aperture on each side. Water enters at the nostril and is pumped back-
wards by a muscular velum through the gill chambers and out behind.
There is also a single posterior oesophago-cutaneous duct on the left
side, which is probably closed during normal respiration but is
opened to allow expulsion of large particles. If the nostril is closed
experimentally with a plug no water enters by the mouth or posterior
apertures but the fish survives well, presumably respiring through the
skin.

124 VERTEBRATES WITHOUT JAWS iv. 19-

The thyroid gland consists of a long series of sacs formed by
evagination from the floor of the pharynx.

Down the sides of the body are pairs of slime glands, able to secrete
large amounts of mucus, which may be protective and is said also to
be produced under the operculum to hasten the end of a dying fish
that the hag has attacked.

A curious difference from the nervous system of lampreys is that
the dorsal and ventral roots join, though the details suggest that the
union is not similar to that found in gnathostome vertebrates. The
brain shows several features of reduction and simplification and no
pineal eyes are present. There is only one semicircular canal in the ear
(p. 109). The kidneys show a more generalized condition than in any
other vertebrate in that the pronephros persists in the adult and is
hardly marked off from the mesonephros, so that an almost continu-
ous series of funnels and glomeruli can be recognized. Moreover, there
is a regular series of mesonephric glomeruli, a pair in each segment.

The development is known only in Bdellostoma, where the egg is
yolky and cleavage partial, leading to the formation of an embryo
perched on a mass of yolk. It is often stated that Myxine is a protandric
hermaphrodite, because individuals are found in which the front end
of the gonad contains eggs, whereas the hind part is testis-like (Fig.
81). No ripe sperms have ever been found in this region, however,
and, moreover, individuals with fully testicular gonads do occur.
Since it is known that in other vertebrates (including the lampreys)
the gonads go through a hermaphrodite stage during development it
seems likely that Myxine is not a functional hermaphrodite but that
the double-sexed gonad shows a rather late persistence of the indeter-
minate stage.

The hag-fishes all live in the sea and their blood differs from that of
other chordates in that it is isosmotic with sea water. However, the
individual ions are regulated; sodium and phosphate exceed their
values in sea water, and the other ions are present in lower concentra-
tion. It is usually assumed that fishes, with their glomerular kidneys,
evolved in fresh water. However, the very earliest fragments of
armoured agnathans are from Ordovician deposits that may be littoral
or marine and it might be that the condition of the blood and kidney
of Myxine is that of the earliest agnathans and that the glomerulus was
not evolved as an adaptation to freshwater life, as is often supposed
(Robertson, 1954).

The organization of the lampreys and hag-fishes shows that they
preserve many characteristics from a very early stage of chordate

IV. 20

FOSSIL AGNATHANS

125

evolution, probably that of about the Silurian period. Their special
interest for us is in giving an insight into the organization possessed
by the vertebrates before jaws were evolved. However, no doubt many
changes have gone on during cyclostome evolution and we must not
suppose that all Silurian vertebrates were like lampreys. Indeed, we
may now complete our picture of this stage of evolution by examining
the fossil fishes known to have existed at that period. We shall find
them superficially so different from modern cyclostomes that only
careful morphological comparison reveals the similarities. The inquiry
will show us once again how a common plan of organization can be
found in animals of very different superficial form and habits.

Fig. 83. A ccphalaspid restored (Hemicyclaspis).

d. dorsal fin; bf. lateral field; pec. pectoral fin; p. pineal; sclr. sclerotic ring.
(From Stcnsio.)

20. Fossil Agnatha, the earliest-known vertebrates

The ostracoderms are fossil forms from freshwater Silurian and
Devonian deposits. They are therefore the oldest fossil vertebrates
known to us (except for a few Ordovician fragments), and this makes
it specially interesting that they show affinity with the cyclostomes.
These are fossils that are rarely found complete, particularly the
pteraspids, but a quarry in Herefordshire yielded numerous whole
specimens of Cephalaspis and Pteraspis of Old Red Sandstone age,
probably all from a single dried-up pool.

In the cephalaspids (Osteostraci) the head was flattened and com-
posed largely of a shield. The rest of the body was fish-like, with an
upturned tail (heterocercal, see p. 136) covered with heavy bony scales
(Fig. 83). A pair of flaps behind the gills may have functioned like
pectoral fins.

On the dorsal surface of the shield are two median holes, one
behind the other, which served a naso-hypophysial opening and a
pineal eye. The whole outline of the cranial cavity is preserved and
shows a brain remarkably like that of a lamprey, with a naso-hypo-
physial canal below it (Fig. 84). There were paired eyes and only two

(126)

eFf.pm

l.br.l

Fig. 84. Head shield of the ccphalaspid Kiaeraspis, see from below. 5 X natural size.

car. a. internal carotid; d.ao. dorsal aorta; eff.br. 4. 4th efferent branchial; eff.pm. efferent branchial

of 1st arch; i.br.i. 1st interbranchial ridge; oes. oesophagus; orb. depression made by orbit; vest.

depression made by vestibular apparatus. V1-X2. Cranial nerves.

(After Stensio.)

hup. foss

orb

■ C3p tat

Mf/m

Fig. 85. Cast of the endocranium and system of canals in the head shield of Kiaeraspis.
amp. ampulla of posterior semicirculr canal; can. canal leading to field; car. a. carotid artery;
hyp.foss. hypophysial fossa; /./. lateral 'electric' fields; med. medulla oblongata; nas.c. naso-
hypophysial canal; orb. orbit; v.cap.lat. vena capitis lateralis; vest, vestibular apparatus; III-X

cranial nerves. (After Stensio.)

iv. 2 o CEPHALASPIDS 127

semicircular canals. Long tubes leading through the shield contained
the cranial nerves, which can be reconstructed in detail (Fig. 85).
On the under side of the shield is a series of ridges, which outline a
set of ten pairs of branchial pouches. The first of these lies far forward
at the sides of the mouth and the ridge in front of it is probably the
premandibular arch; it carries the profundus nerve (p. 152), which
was large. The ventral surface of the head was flat and covered with
small scales. Probably the gills were pouches, as in lampreys. The
canals of the aorta, epibranchial arteries, and some features of the veins
and heart have been preserved.

The mouth was a slit at the extreme front end with which the
animals may have scooped decaying matter from the lake floor.
On the dorsal surface there are sunken areas, covered by small scales,
known as the median and lateral fields, and supposed by some to have
contained electric organs. They were apparently served by a very rich
blood-supply and a system of wide canals leads to the vestibular
region. These canals might have contained nerves, but Watson makes
the far more likely suggestion that they housed tubular extensions of
the labyrinth and served to carry pressure waves to the ear, perhaps
providing a substitute reinforcement for the defective lateral line
system.

We therefore know in some respects as much about these fossils as
of many living fishes. They show in the complete segmentation of the
head the most primitive condition known among craniates. Many of
their features are very like those of modern lampreys and there can be
little doubt that, as Stensio suggests, the latter represent their sur-
viving descendants, which have lost the bony shield.

The Anaspida (mostly Silurian) are placed by Stensio near the
Cephalaspids but they are less well known. They were small fishes
(up to 7 in. in length) covered with rows of bony scales (Fig. 87). The
tail shows a lower lobe larger than the upper ('hypocercal'). This
would presumably serve to drive the head end upwards perhaps to
compensate for the weight of its armour. The opposite ('heterocercal')
condition, found in cephalaspids and many modern fishes (for
instance, the dogfish), produces a tendency to negative pitch and is
associated with the presence of pectoral fins (p. 136). The anaspids
possessed a curious ventral or ventro-lateral fin fold (Fig. 87) or
perhaps a series of them. There were large paired eyes, median holes
presumed to be nasal and pineal and a series of up to fifteen small
round gill openings.

We may consider here the fossil Jamoytius from the Silurian. The

i 2 8 VERTEBRATES WITHOUT JAWS iv. 20

notochord was persistent and there was no calcined endoskeleton.
There were long continuous lateral fin folds and a hypocercal tail. A
series of transverse structures were at first interpreted as myotomes

Pterolepis

Rhyncholepis

sec/.

pec.

Rhyncholepis

Figs. 86 and 87. Anaspids seen in dorsal and lateral views.

an. anal fin; na. nasal aperture; orb. orbit; pec. pectoral spine; pi. pineal foramen;
ros. rostrum; sc.d. dorsal scales. (After Stensio and Kiaer and Grasse.)

but Stensio and Ritchie (i960) consider these to be scales and place
Jamoytins with the Anaspida. In either case, the form is of the greatest
interest, and represents as White says 'the most primitive of the
"vertebrate" series of which we have knowledge'. It is suggested that
it might be the ammocoete larva of an ostracoderm (Newth).

The Heterostraci are actually the oldest known craniates, since their
scales occur in the Ordovician. They were common in the Silurian

IV. 20

HETEROSTRACI

129

and lower Devonian. There were ventral as well as dorsal shields (Fig.
88), and a long series of gill pouches, but only a single pair of exhalent
branchial apertures, suggesting to Watson respiration by a moving
flap (velum). The shields were of cell-less bone (isopedin) covered
with dentine. The body was covered with scales of similar material.
The tail was hypocercal and there were lateral horizontal keels but
no fins. Theie were paired eyes, two semicircular canals and clearly

Fig. 88. Three views of a restoration of Pteraspis.
d.sp. dorsal spine; e. eye; m. mouth; r. rostrum. (From White.)

marked lateral line canals. There was a pineal opening, closed in the
adult, but no sign of the nostril, which may have opened into the
mouth. The latter was surrounded by long plates, suggesting that it
formed a protrusible apparatus, which could be pushed out to form
'a kind of scoop or shovel (Fig. 88) whereby mud and decaying refuse
could be taken off the bottom, for it seems likely that such were their
food and habit' (White).

The coelolepids or thelodonts are the least known group of agna-
thans. The outer surface was covered with fine, placoid-like scales or
hollow spines, which in isolation are often found in late Silurian and
Early Devonian rocks. The anterior end was usually flattened and
wide but the body behind was narrow, with a forked, probably
hypocercal tail. Structures that are probably eye-spots occurred
widely separated near the front margin. The mouth was ventral and
traces of seven branchial arches have been found. There were flap-like

i 3 o VERTEBRATES WITHOUT JAWS iv. 20

extensions on each side of the head but no paired fins. The only
median fin was the anal.

The affinities of these ostracoderm fossils with each other and with
the cyclostomes have been much disputed. Lankester claimed that
pteraspids were related to cephalaspids 'because they are found in the
same beds, because they have a large head shield and because there is
nothing else with which to associate them'. At the other extreme
Stensio holds that we have sufficient evidence to assert that the
pteraspids have given rise to the myxinoids, and the cephalaspids to
the lampreys. Except for the absence of jaws there is indeed little in
common among the fossil forms. The differences in the shape of the
tail are especially baffling. As White points out, an animal with a
heterocercal tail and pectoral fins can hardly have lost either of these
organs independently. He suggests that the earliest vertebrates pos-
sessed straight ('diphycercal') tails and that from these were evolved
on the one hand the pteraspids with hypocercal tails and on the other
the cephalaspids with upturned heterocercal tails. The modern cyclo-
stomes are perhaps derived from the latter, but which, if either, group
gave rise to the earliest gnathostomes is unknown.

The Agnatha were the first animals of the chordate type to become
large, and they apparently all did so by feeding on the detritus at the
bottom of rivers and lakes. They evolved into various types, mostly
rather heavily armoured and perhaps slow-moving forms. The lam-
preys and hag-fishes have been derived from early Agnatha by the
evolution of a sucking mouth, perhaps with loss of the bony skeleton
and paired limbs. However, it was the unknown forms that evolved
a biting mouth that made the next great advance in vertebrate
evolution.

THE APPEARANCE OF JAWS.
THE ORGANIZATION OF THE HEAD

1 . The elasmobranchs : introduction

In all parts of the sea there are to be found members of the class of
the elasmobranchs (literally 'plate-gilled' fishes), including sharks
ranging from monsters of 50 ft long to the common dogfish Scylio-
rhinus caniculus of 1-2 ft. Nearly all the fishes in the group are carni-
vorous or scavengers: the skates and rays are bottom-living relatives,
feeding mostly on invertebrates. Although they are not quite so fully
masters of the water as are the bony fishes, they are yet well enough
suited to that element to survive in great numbers in all oceans.
Perhaps the skill and cunnning of a shark is exaggerated by the
frightened boatman or bather, who is apt to mistake a keen nose and
the persistence of hunger for intelligence, especially when he is faced
at intervals with a well-armed mouth; but the sharks have a large
brain and their active, predacious habits enable many of them to
live by eating the more elaborately organized bony fishes.

Evidently such active creatures have changed considerably if they
have been evolved from the heavily armoured and probably slow-
moving agnathous vertebrates that shovelled up food from the bottom
of Palaeozoic seas. It used to be supposed that these elasmobranch or
cartilage fishes represent a very primitive stock, but we now realize
that there have been great changes since the biting mouth was first
evolved; we cannot be sure that any features we find in the elasmo-
branchs were possessed by the earliest gnathostomes.

The typical shark is a long-bodied fish, swimming by the passage of
waves of contraction along tne metamerically arranged muscles. As in
the lampreys and eels, the wave that passes down the body is of short
period, relative to the length of the fish, and is therefore evident as it
travels along. This is probably a less efficient system than is provided
by the longer period waves of the most highlv developed bonv fishes;
the sharks are good swimmers, but except for the mackerel sharks
(Isuridae) not among the swiftest. Stability and control of direction
are ensured by the upturned tail and the fins. The tail, with its dorsal
lobe larger than the ventral, is called heterocercal, and tends to drive
the head downwards. This is corrected by the flattened shape of the
head itself and by the pectoral fins, which act as 'aerofoils', allowing

i 3 2 THE APPEARANCE OF JAWS v. i-

steering in the horizontal plane (p. 140). There are two dorsal fins,
which secure stability against rolling, and also assist in making possible
the vertical turning movements.

The muscles for the production of these movements are a serial
metameric set, with longitudinal fibres, essentially like those of the
lamprey or amphioxus. The central axis is no longer simply a rod;
the notochord has become surrounded and partly replaced by a series

df f s P .by Ld

ac.

bw.

msv. pr b.

Fig. 89. Diagram of the organization of a vertebrate.

ac. wall of abdominal coelom ; b. body wall ; bd. basidorsal ; bv. basiventral ; bw. body wall ; dr. dorsal

rib; i. intestine; iv. interventral; m. myocomma; ms. mesentery; msd. median dorsal septum; msv.

ventral mesentery; nes. neural tube; ns. notochordal sheath; pr. ventral (pleural) rib; sp. neural

spine; ts. horizontal septum. (From Goodrich.)

of vertebrae (Fig. 89). These develop as two pairs of cartilaginous
nodules in each segment, the basidorsals and basiventrals behind, and
smaller elements, the interdorsals and interventrals, in the front. The
basiventrals, lying on either side of the notochord, form the centrum
of each vertebra, invading and almost interrupting the notochord,
which widens again, however, between the vertebrae. The vertebrae
are held together by ligaments, but are not articulated by complex
facets as they are in land animals. The basidorsals form neural arches
above the nerve-cord, and the interdorsals make intercalary arches.
The interventrals partly separate the centra. Attached to each basi-
ventral is a pair of transverse processes, which in the anterior region
bear short ribs and in the tail are fused in the midline to make the
haemal arches.

The median and paired fins are supported by cartilaginous rods,
the radials, and their edges are further strengthened by special horny

SWIMMING OF FISHES

i33

rays, the ceratotrichia. The radials of the paired fins form a series
attached to larger rods at the base. These more basal rods are attached
to a 'girdle' of cartilage embedded in the body wall. The pectoral

Fig. 90. Successive positions of a swimming dogfish at intervals of o-i sec. The
lines are 3 in. apart. The passage of a wave is marked by dots. (After Gray.)

Fig. 91. Successive positions of a swimming eel at intervals of 005 sec. Scale 3 in.
The wave-crests are marked. (After Gray.)

girdle is a hoop extending some way round the body, but the pelvic
girdle is simply a transverse rod in the abdominal wall. The origin of
these girdles and of the fins will be discussed later (p. 136).

2. The swimming of fishes

The propulsive forces that move a fish through the water are usually
produced by the longitudinal muscle-fibres of the myotomes, but in
some forms the propulsion is produced by movement of the fins,
whose function is usually rather to give the fish its stability, enabling it
to keep on a constant course, and also to change its course.

i 34 THE APPEARANCE OF JAWS v. 2

The myotomes consist of blocks of longitudinal muscle-fibres,
placed on either side of an incompressible central axis, the notochord

or vertebral column. The effect of
contraction of the muscle-fibres in any
myotome is therefore to bend the body.
In forward swimming the contraction
of each myotome takes place after that
in front of it. In this way waves of
curvature are passed down the body,
alternately on each side. This can be
illustrated by a series of photographs
of a fish such as the dogfish or eel in
which the amplitude of the waves is
large (Figs. 90 and 91).

In other fishes the waves are not so
immediately obvious, but serial photo-
graphs show that even in such forms as
the mackerel and whiting there is a
backward movement of waves. The
number of waves per minute in steady
swimming varies from 54 in the dog-
fish to 170 in the mackerel, the
corresponding velocities of the waves
being 55 and 77 and of the whole fish
29 and 42-5 cm /sec.

Gray has shown how the muscle
contractions produce movements of
the parts of the body, related to one
another in such a way as to transmit
a backward momentum to the water.
Fig. 92 shows superposed drawings of
an eel, made from successive photo-
graphs. The region marked XY is
moving from right to left and that
X 1 Y 1 from left to right and evidently,
as Gray puts it, 'all parts of the fish's
body which are in transverse motion have their leading surfaces directed
backwards and towards the direction of transverse movement, but
the angle of inclination is most pronounced when the segment is
crossing the axis of longitudinal motion, and at this point the segment
of the body is travelling at its maximum speed. Each point of the body

Fig. 92. Enlarged drawings of suc-
cessive photographs of a young eel
superimposed on each other so that
the tips of the head are on the same
transverse axis and the longitudinal
axes of motion (ab) are made to
coincide. As the wave passes the
section XY it first moves to the left
and is directed backwards and to
the left, whereas X x Y\ moves
in the opposite direction. The tip
of the tail follows a figure of 8.
(From Gray)

v. 2 SWIMMING OF FISHES 135

is travelling along a figure 8 curve relative to a transverse line which is
moving forward at the average forward velocity of the whole fish.
The track of any point on the body (relative to the earth) is a sinu-
soidal curve whose pitch or wave length is less than that of a curve
which defines the body of the fish. There is therefore a definite angle
between the surface of the fish and its path of motion.'

Each portion of the side of the fish can thus be considered as moving
like the blade of an oar used for sculling at the back of a boat. The
principle used, that of an inclined plane, is the same as in screw pro-
pulsion, the essential feature being that the moving surface is inclined
at an angle to its line of motion. The effect of the movement is greatly
increased by the fact that the amplitude of the oscillations grows
passing backwards, as is necessary to produce additive effects in any
coupled system of screws or turbines. The whole fish thus operates
as a single self-propelling system.

The magnitude of the forward thrust thus generated depends
among other things on (a) the angle that the surface of the fish makes
with its own path of motion, (b) the angle between the surface of
the fish and the axis of forward movement of the whole fish, and
(c) the velocity of transverse movement of the body (Gray). These are
evidently factors that will vary with the shape of the body and the
action of its muscles. The body form of the faster-moving types of
bony fishes provides substantial advantages for swimming over that
of the more elongated types. The essential differences are that the
bony fishes have (1) large caudal fins, (2) a much smaller length of the
body relative to its depth, (3) less flexibility.

The role of the large caudal fin is to resist transverse movements;
its effect is, again quoting Gray, 'to keep the leading surface of the
body directed obliquely backwards during both phases of its trans-
verse movements and thereby to exert a steady pressure on the water'.
Since, however, the tail does execute transverse movements, and at
the same time is being rotated towards and away from the axis of
motion, it exerts a very large propulsive effect, probably as much as
40 per cent, of the total thrust.

The effect of the caudal fin, combined with the shortness of body
and reduced flexibility, is that the front part of a bony fish makes only
small transverse movements; the track of the head is therefore nearly
straight and the whole front of the body presents a streamlined
surface with little resistance. Further, the muscles just in front of the
tail exert their tension with very little change in length.

No doubt the shape of the body also has an important influence on

136 THE APPEARANCE OF JAWS v. 2-

the effect of the fish on the water and hence on the turbulence in the
flow of water and the resistance that must be overcome. Gray has
shown that in a dolphin the resistance cannot be that of a rigid model
towed at the speed at which the animal moves, since this would require
that the muscles generate energy at a rate at least seven times greater
than is known in the muscles of other mammals. By watching the
flow of particles past the body of fish-like models he showed that
movements such as those produced in swimming accelerate the water
in the direction of the posterior end, and this would greatly reduce
the turbulence.

Something is known of the nervous mechanism responsible for the
production of the swimming waves. An eel can swim if its whole skin
has been removed. If a region of the body is immobilized by a clamp,
swimming waves can pass along. Therefore the rhythm is determined
by some intrinsic activity of the spinal cord and not by any mechanism
such as proprioceptor impulses arising in active muscles and causing
others to contract.

Experiments in which the spinal cord was cut across show that in
the eel the rhythm is only initiated when suitable impulses reach the
cord either from spinal afferents or from the brain. Thus the spinal
eel can be made to swim either by fixing a clip on to its caudal fin or by
electrical stimulation of the cut end of the spinal cord. Though the
cord requires such afferent stimuli for its functioning, they do not
determine the frequency of the rhythm, which bears no relationship
to that of the applied stimuli.

In the dogfish the isolated spinal cord is able to initiate rhythmic
swimming. After transection behind the brain the posterior portion
of the fish exhibits continuous swimming movements for many days.
Light touch on the sides of the body inhibits these movements, but some
sensory impulses are necessary for their initiation; after complete de-
afferentation, by section of all the dorsal roots, the movements cease.

The information available does not yet enable us to understand
fully how the swimming rhythm is initiated and maintained, nor how
it is influenced by the brain. It would be very interesting to have
further knowledge on these topics, especially because the locomotor
rhythms of land animals are probably based on the serial contractions
of their fish ancestors.

3. Equilibrium of fishes in water ; the functions of the fins

Making use of the methods of investigation of aeronautical engineers,
studies have been made of the forces that operate to keep a fish stable

v. 3 EQUILIBRIUM OF FISHES 137

as it moves through the water, or allow it to become temporarily un-
stable and hence to change direction. Instead of attempting to study a
living or dead fish moving in water, Harris made models and supported
them in a wind-tunnel in an apparatus suitable for measuring the
forces at work in the various directions. Such a method, in which no
compensating movements of the fins are allowed, makes it possible
to investigate the so-called 'static stability' of the fish, that is to say,

Fig. 93. Diagram of model of the dogfish Mustelus, showing the conventional terms
for describing deviations of motion. The longitudinal axis X is that of the wind
tunnel and Y (horizontal) and Z (vertical) are at right angles to it. The arrows show
the directions known as positive rolling, pitching, and yawing, which occur about the
X, Y, and Z axes respectively, a. is the angle of attack between the axis of the model
and the X axis. (From Harris, J. exp. Biol. 13.)

to see whether the body and fins are so shaped as to provide forces
that tend to bring the fish back into its previous line of movement after
it has deviated in any direction. Any body such as a fish or aeroplane
is said to be in stable motion if when it veers slightly from its line of
progress the new forces produced upon its planes tend to restore the
original direction of motion.

The forces acting on the fish are measured along three primary axes,
longitudinal, horizontal, and vertical. Deviation from the line of
motion about the longitudinal axis is known as rolling, about the
transverse axis as pitching, and about the vertical axis as yawing
(Fig. 93). The forces along these three axes are known as drag, lateral
force, and lift.

In order to discover the effect of the median fins and tail on the
stability, these fins were removed, the heterocercal tail being replaced
by a cone having the same taper as the actual caudal fin. The model
was then placed in the wind-tunnel with a wind at 40 m.p.h., which

138 THE APPEARANCE OF JAWS v. 3

corresponds to a motion of 3 m.p.h. in water. The lateral force was
measured when the body was made to yaw at various angles. The

+0-2
+ 0-1

-15 -ipl^^ f

-0

-0-2

+5° +10° +15°

+ 5" oX S+Yo° +iV

+ 6

+ 05

+0-4/

/o-z

+03
*0-1

+5° +10*

+15

-0-1

-04

-0-5

Fig. 94. A. Results of yawing test on model of Mustelus without fins. The lateral force
is plotted as a light full line, drag force as a light broken line; yawing moment about
centre of gravity as full heavy line. Abscissae show the angle of attack in degrees,
ordinates the lateral force and drag in pounds weight, yawing moment in in. -lb. X ^j.
n. Yawing test similar to (a) but with the fins behind the centre of gravity in place.

C. Yawing test with all median fins in place.

D. Pitching test on model of Mustelus with all fins intact and pectoral fins set at an
angle of incidence of 8°. Lift force is shown as a light full line, drag force as a light
broken line, pitching moment about the centre of gravity as a heavy full line.

(From Harris.)

results showed that the equilibrium in this plane is quite unstable; a
slight turn off the direct course would produce a turning moment
tending to increase still further the deflection (Fig. 94). This is a
well-known property of all airship hulls, and is known as the 'unstable
moment' of the hull. It is corrected in the airship by the addition of

v. 3 FUNCTION OF FINS 139

suitable horizontal and vertical fin surfaces at the rear end, when the
airship becomes in effect a feathered arrow. The forces operating on
the fins tend to bring the body back into the original line of motion.
The fins of the fish operate in a similar manner. If the experiment
is performed with a model to which all the fins behind the centre of
gravity have been added, namely, the caudal, anal, and second dorsal
fins, it is found that the curve for the yawing moment now has a steep
negative slope (Fig. 94 b), that is to say, every deviation produces
forces that tend to give directional stability. With the first dorsal fin
also in position the model possesses a remarkable neutral equilibrium
(Fig. 94 c). Deviations by as much as io° produce no resultant yawing
moment about the centre of gravity. The form of the dorsal fins is
therefore definitely such as to maintain stable swimming and prevent
yawing.

Turning of a fish is produced either by the propagation of a wave-
down one side only of the body or by asymmetrical braking with the
pectoral fins (see below). The former type of turn has been investi-
gated by Gray in the whiting, where there is a large caudal fin. This
gives great lateral resistance, so that the first part of the turn is
executed by bending the front part of the fish on the tail as a fulcrum.
This enables the animal to turn through 180 within a circle of the
diameter of its own length. After removal of the caudal fin the turns
are much less effective.

In both elasmobranchs and teleosts the dorsal fins are well developed
in the active swimmers. In most elasmobranchs they are fixed, but in
many teleosts the dorsal fin can be folded up and down, and it is
observed that the fin is raised during turning. This would have the
effect of increasing the yawing moment produced by asymmetrical
action of the body muscles or by unilateral braking with the pectoral
fins.

Since the body is so markedly flexible in the lateral plane and there
are powerful muscles available for turning it in this direction,. the part
played by the fins in determining the stability is important mainly
when the body is held straight. The fish thus has the double advantage
of great stability (by keeping the body straight) and great control-
lability (by bending it). In a body unable to change its shape in this
way, stability and controllability would be inversely related. This is
the case for the stability of the fish in the vertical plane, in which the
body is little flexible. Fig. 94 n shows the positive slope of the curve
for the pitching moment and clearly the equilibrium in this plane is
quite unstable. The pectoral fins contribute more than any others to

Ho THE APPEARANCE OF JAWS v. 3-

movement in this plane, and since they lie in front of the centre of
gravity they greatly increase the instability. The fish must be able to
alter direction in the vertical plane, and it has apparently sacrificed
static stability for controllability. The equilibrium in this plane is a
dynamic one, controlled by the movable pectoral fins, and it is so
unstable that only a small movement of these fins is necessary to
produce a deflecting force that restores the original direction of
motion.

The pectoral fins, lying in front of the centre of gravity, tend to
produce a movement of positive pitch, that is to say, they force the
head upwards. This effect is normally compensated by a component
produced by the heterocercal tail. The upper lobe of this is rigid and
the lower more flexible, therefore the lateral motion given by the
swimming movements of the body produces a vertical lift force on the
tail, giving, of course, negative pitch. After amputation of the hypo-
caudal lobe and anal fin a dogfish swims continually along the bottom
of the tank : in order to compensate for the absence of negative pitch
the pectoral fins are held horizontally and hence there is no moment
to counteract the weight of the fish. If the pectoral fins are then also
removed the anterior end of the body is pointed upwards, often so
much so as to cause the fish to swim with its head out of the water.
This is the result of an over-strenuous attempt to compensate, by
raising the head, for the negative pitch produced by the tail. The
system is no longer suitable for making the continuous adjustments
necessary to ensure stability.

This analysis makes it clear why a heterocercal tail is found in
almost all the primitive swimming chordates; it is almost a necessity
for an animal with a specific gravity in excess of the medium and little
flexibility in the vertical plane. The component of positive pitch
could be provided by the flattened head or by continuous lateral fin
folds, such as may have been present in early fishes, and adjusted
by the limited flexibility possible in the fin. The development of
movable pectoral fins confers much greater control. Since the useful
portions of a fin fold for this purpose would be those well in front of
and behind the centre of gravity, we can perhaps see the reason why
the intervening portion has become lost. In the modern sharks the
pelvic fins have little influence on the stability and are perhaps retained
only for their modification as claspers.

It is not surprising that races of fishes with stability ensured by
systems of this sort should tend to adopt a bottom-living habit, with
dorso-ventral flattening, such as is found in the skates and rays.

v. 4

SKIN OF ELASMOBRANCHS

141

Expansion of the front end is developed at first to compensate the
effect of the tail, but the pectoral fin becomes expanded to allow ver-
tical adjustments and then reduction of the hypocaudal lobe of the tail
accompanies the adoption of life on the sea bottom. Eventually all

Fig. 95. Development of denticles in the dogfish.

A and b, first gathering of odontoblasts (sc.) below the basement membrane (brn.); ml. are the

epidermal cells that will become modified, c, first deposition of dentine (d.). In D there is

more dentine and a pulp cavity (p.) is seen. In E are shown stages in the formation of enamel

(e.) and of the basal plate (bp.) while the denticle cuts the epidermis (ep.).

(From Goodrich, Vertebrata, A. & C. Black, Ltd.)

locomotion is produced by undulatory movements of the fins, which
were at first used only to raise the fish off the bottom.

4. Skin of elasmobranchs

Being swift and predatory animals, more attackers than attacked,
the sharks do not possess a very heavy external armament. The skin
itself is tough, being covered by layers of epidermis. Beneath this is a
thick dermis of connective tissue with fibres arranged at right angles

142 ORGANIZATION OF THE HEAD v. 4-

as in a carpet, giving a tissue of great strength and flexibility, able to
maintain the shape of the body. Scattered over the skin are the charac-
teristic denticles or placoid scales (Fig. 95). Each of these consists of a
pulp cavity, around the edge of which lies a layer of odontoblasts
secreting the calcareous matter of the scale, known as dentine. This
has a characteristic structure resulting from the fact that the odonto-
blasts send fine processes throughout its substance. The outside of the
dentine is covered by a layer of enamel, secreted by the overlying
ectoderm. Usually the denticles pierce through the ectoderm, after
which no further enamel can be added to their surface. Obviously the
scales are similar to teeth, which are indeed to be considered as
specialized denticles developed on the skin of the jaws. It has often
been supposed that the denticle is the primitive type of fish scale,
from which others have been derived, but it now seems more likely
that the earliest covering was a continuous layer, later broken into
large scales, from which the denticle was ultimately derived (p. 269).
The skin also gives protection to the fish by its colour, produced
by a layer of chromatophores beneath the epidermis. Many sharks
have a spotted or wavy pattern, which breaks up their visible outline
as they move in the water, especially near the surface. They are able
to change their colour, though only slowly, becoming darker on a dark
background (see p. 164).

5. The skull and branchial arches

In general organization a dogfish follows closely the fish plan,
which we have already considered. Most of its special new features
are in the head, and we may now turn to a consideration of the
organization of the head and jaws of a gnathostome vertebrate. The
jawless vertebrates of the Silurian and Devonian included fresh-
water animals of various sorts, but the vertebrate type began to
flourish and increase more abundantly with the appearance of creatures
with jaws in the late Silurian. From this stage onwards we have to
follow the parallel history of numerous orders and families, as the
vertebrate plan of structure became adapted for various habitats. It
seems likely that the development of a biting mouth greatly increased
the range of possibilities of vertebrate life. The most obvious use of
a mouth is for attacking other animals, but it may also have been used
to collect plant food from all sorts of situations where it would not
be available to the microphagous or shovelling Agnatha. Probably the
mouth was also early used for defence, and in this way influenced the
whole bodily organization, making unnecessary the heavy armature

v. 5 DEVELOPMENT OF THE JAWS 143

that is so characteristic of many early vertebrates. Modern research
has shown that the armour has become progressively reduced along
various lines of iish evolution. Older ideas of comparative anatomy
regarded the 'cartilage fishes' as showing a primitive stage, preceding
the appearance of bone. We now realize that this is the opposite of the
truth and that the dogfish and its relatives represent a higher type,

rosC

Fig. 96. Skull and branchial arches of the dogfish (Scyliorliimts).
au.c. auditory capsule; b.b. basibranchial; b.li. basihyal; c. centrum; cer.b. ceratobranchials;
cer.h. ceratohyal; d.r. foramen for dorsal root; e.b. extrabranchials; e.c.f. external carotid
foramen; e.l. ethmoid ligament; ep.b. epibranchials; gr. groove for anterior cardinal sinus;
g.r. gill rays; hy.a. foramen for hyoid artery; hymd. hyomandibula; i.d. interdorsal; io.c.
interorbital canal; I.e. labial cartilages; M.c. Meckel's cartilage; na. neural arch; nas.c. nasal
capsule; o.n.f. orbito-nasal foramen; op. foramen for ophthalmic nerve; op.g. groove for
op.V; op.V, op. VII ophthalmic branches of V and VII; orb. orbit; ph.b. pharyngobranchials ;
p.sp.l. prespiracular ligament; r. rib; rost. rostral cartilages; spd. supradorsals ; tr. transverse
process; vr. foramen for ventral root; II-IX, foramina for cranial nerves. (After Borradaile.)

able to defend themselves by mobility, by biting, and by efficient
sensory and nervous organization. Heavy defensive armour is a
primitive form of protection for animals, as for man.

Besides its use in feeding and defence, the mouth can also be used as
a means of 'handling' the environment, for instance in the nest-build-
ing activities of many fishes. Indeed, it is difficult for us to realize the
utility of the jaws for an animal not provided with any other means of
seizing hold of objects.

The development of the mouth to a point at which it could be used
in these varied ways was, therefore, a very important stage in evolution.
Recognition of the Gnathostomata as a separate group of animals is
far more than a matter of classificatory convenience, it marks the
achievement of the possibility of life in a greatly increased range of
environments.

144 ORGANIZATION OF THE HEAD v. 5-

Morphological analysis enables us to see how this biting mouth
was produced, by modification of one or more of the gill-slits. The
main differences that separate the gnathostome from cyclostome ver-
tebrates are therefore in the head and its skeleton. Although the
modern elasmobranchs show the skull and jaws in a modified and
reduced condition, they provide by their simplicity a good starting-
point for discussion. The 'skull' of a dogfish consists of a series of

ac.

pan

--dao

Fig. 97. Diagram of skull of selachian embryo before fusion of the main cartilages;
cranial nerves black, numbered; arteries cross-lined.

ac. auditory capsule; bra. epibranchial; dao. dorsal aorta; eps. efferent pseudobranchial;

ha. efferent hyoid; hv. hypophysial vein; i.e. internal carotid; nc. nasal cartilage; oc. orbital

cartilage; oca. occipital arch; op. optic; oph. ophthalmic; or. orbital; pan. pila antotica; pf.

profundus nerve; pch. parachordal; poc. polar cartilage; tr. trabecula. (From Goodrich.)

cartilaginous boxes surrounding the brain and receptor organs (Fig.
96). The nasal capsules, orbital ridges, and auditory capsules are
largely fused with the main cranium, producing a single continuous
structure, the chondrocranium. It is interesting to consider how this
structure has arisen during the process of cephalization. Presumably
parts of it represent the modified sclerotomes of trunk regions. We
shall see presently that there is strong evidence that the head has arisen
by modification of a segmental arrangement such as is seen in the
trunk; the morphogenetic processes that build the skull must there-
fore be related in some way to those of the vertebrae. The first rudi-
ment of the skull in the embryo consists of two pairs of cartilaginous
rods, the parachordals and trabeculae (Fig. 97). The former lie on
either side of the notochord, the trabeculae in front of the notochord.
These first rods fuse up to make a continuous plate; from this grow
sides and roof, completing the cartilaginous neuro-cranium around the
brain. Meanwhile cartilaginous capsules form around the nose, eyes,
and ears, and become joined to the neuro-cranium. Posteriorly, behind

v. 6 BRANCHIAL ARCHES 145

the auditory capsules, the cranium is completed by the addition of a
number of segmented elements, evidently modified vertebrae.

The problem is, therefore, to determine the nature of the pro-otic
part of the skull. Before we can settle this we must consider the
visceral or branchial arches. These are pairs of rods of cartilage
developed in the walls of the mouth and pharynx, between the gill-
slits. In the dogfish each typical branchial arch (Fig. 96) consists of a
series of four pieces, the pharyngo-, epi-, cerato-, and hypo-branchials.
Ventrally some of the arches join a median basibranchial plate. These
rods lie in the pharynx wall and on their outer sides carry a series of
projecting rods, the branchial rays and extrabranchial cartilages,
whose function is to support the lamellae of the gills.

There are five such branchial arches, differing only slightly from
each other. In front of these lie two arches, the hyoid and mandibular,
which, though modified, are obviously of the same series. The hyoid
the more nearly resembles a typical branchial arch. Its most dorsal
element, the hyomandibular cartilage, is a thick rod attached dorsally
to the skull by ligaments and at its lower end forming the support
for the hind end of the jaw. It apparently corresponds to the epi-
branchials. The more ventral elements, cerato- and basihyal, resemble
the corresponding members of more posterior arches. The jaws them-
selves (mandibular arches) depart more widely from the form of a
typical branchial arch, but the two thick rods of which each is com-
posed, the upper palato-pterygo-quadrate bar and the lower Meckel's
cartilage, are recognizably members of the branchial series. Looking
at the whole apparatus with a thought to the embryological processes
that have produced it, with as it were a manufacturer's eye, we can
see at once that the jaws and hyoid arch have been produced by a
modification of the processes that make the branchial arches.

6. The jaws

Study of the serial relationship of the jaws and branchial arches
gives us an understanding of the course of evolution of the mouth.
We may suppose that the ancestors of the gnathostomes possessed a
nearly terminal mouth, either on the front end of the body or on the
ventral surface. The pharynx was pierced by a series of gill pouches,
beginning shortly behind the mouth and separated by arches, each
containing a set of cartilaginous bars (Fig. 96). There is some evidence
that this condition persisted in the cephalaspids (p. 125), where there
is found to be a series of ten pairs of gill-slits, beginning far forward
on either side of the mouth. The muscles moving the more anterior

146 ORGANIZATION OF THE HEAD v. 6

parts of the pharynx wall and the anterior arches could be called into
play to help in the collection of food. In this way the mouth came to
be used for prehension, and the grasping jaws of the gnathostomes
appeared as the more anterior arches became modified to allow more
efficient seizing, and the skin over them was modified to form the
teeth. The mouth probably shifted backwards during this process and
its lateral edges joined the first gill-slit. The rods supporting the
posterior wall of that slit thus became bent over into the characteristic
position of the vertebrate jaws.

There is some uncertainty as to the means of support of the jaws
in the earlier stages of their evolution. The front end of the palato-
pterygo-quadrate bar is attached to the cranium in the dogfish by the
ethmo-palatine iigament'. In most elasmobranchs the hind end of the
upper jaw is not fixed to the cranium but is slung from the latter by
the hyomandibula and by a prespiracular ligament. This means of
support, known as hyostylic, was for long supposed to have been the
original one. But the earliest gnathostomes (the acanthodians) do not
have this arrangement (p. 187), indeed, their hyoid arch is an almost
typical branchial arch, not modified to support the jaw. In the primi-
tive condition one would not expect the hyoid arch to have any con-
nexion with the mandibular. In the acanthodians the jaw is supported
by direct attachments to the cranium at its hind as well as front end,
a condition known as autodiastylic.

The early elasmobranchs themselves do not have a hyostylic jaw
support, but an arrangement in which the upper jaw is both attached
to the cranium and also supported by the hyomandibula. This
amphistylic condition persists to-day in the primitive shark Hexan-
chus. Apparently the jaws, which at first swung from the skull, later
became fixed at the hind end to the hyoid, and this finally became the
only means of support posteriorly. The advantage of this last arrange-
ment is presumably that it allows a wide gape for swallowing, the prey
whole. As the sharks sought to eat larger and larger fishes, those in
which the hind end of the upper jaw was less firmly fixed to the skull
were the more successful and so the hyostylic condition was achieved.

If this theory of the origin of the jaws is correct we may expect to
find some trace of a cartilaginous support for the side wall of the
pharynx in front of the original first gill-slit, a premandibular visceral
arch. Many sharks have two pairs of labial cartilages in this position,
which have been held to represent arches. However, there are strong
grounds for believing that this is represented by the trabeculae cranii,
the rods lying on each side in front of the parachordals and contribut-

v. 6 ORIGIN OF THE JAWS 147

ing to the floor of the skull (Fig. 98). Many points indicate that these
rods are not part of the axial skeleton. The main axis of the body
presumably ends at the front end of the notochord, that is to say, at
the level of the front ends of the parachordals. Indeed there is much
confirmatory evidence to show that this level represents the end of the

^ 12.2m R £

gsX rn.a.'ka'.'*br.a.l" 9 s - 9
Yt ¥2,3.

gut

FlG. uS. Diagrams to show the condition of the visceral arches and
jaws in early vertebrates.
A. cephalaspid; B. acanthodian; C. elasmobranch. (i.e. auditory capsule;
"br. a. 1" first branchial arch; c.n.c. nerve-cord; e. eye; gs. I. first gill-slit;
//. hypophysis. /i.a. hyomandibular arch; m. a. mandibular arch; m. mouth; not.
notochord; p.m.a. premandibular arch (trabecula); sp. spiracle; Vi, pro-
fundus nerve; V2, 3, trigeminal nerve; VII, facial; IX, glossopharyngeal;
X, vagus. (Modified after Westoll.)

segmented part of the body, everything in front of this level being as
it were pushed forward from above or below. The trabeculae have
exactly the relations to the most anterior nerves and blood-vessels
that would be expected of visceral arches. Confirmation of the theory
comes from the discovery that the cartilage of the front part of the
trabeculae, like that of the visceral arches, is formed by material
streaming down from the neural crest, that is to say, from ectoderm.
The branchial arches, hyoid, jaws, and trabeculae thus all constitute
a single series, the result of the working of a repetitive or rhythmic
process, appropriately modified at each level.

148 ORGANIZATION OF THE HEAD v. 7-

7. Segmentation of the vertebrate head

The rhythmicity or metamerism seen in the cartilages can be traced
throughout the structure of the head. Although in higher vertebrates
the head appears as a distinct structure, separated from the body by
a neck, yet there is every reason to think that it has arrived at that
state by gradual modification of the anterior members of an originally
complete metameric series. The jaws, the receptor-organs, and the
brain have become developed at the front end of the body, producing
what zoologists conveniently if pretentiously call cephalization.

The fundamental segmentation of the head is not very easily appar-
ent to superficial observation; the working out of its details is an
excellent exercise in morphological understanding. Recognition of the
segmental value of the various structures also makes them the more
easily remembered. For instance, the nerves found in the head have
been named and numbered for centuries by anatomists in an arbitrary
series:

I. Olfactorius
II. Opticus

III. Oculomotorius

IV. Trochlearis (patheticus)
V. Trigeminus

VI. Abducens
VII. Facialis
VIII. Acousticus
IX. Glossopharyngeus
X. Vagus
XI. Accessorius
XII. Hypoglossus

Morphological study has shown that these nerves are not isolated
structures, each developed independently, but that they represent a
regular series of segmental dorsal and ventral roots of the head
somites. The satisfaction and simplification given by this generaliza-
tion is one of the clearest advantages of morphological insight. More
important still, such understanding of the morphology of a structure
shows us how to look for the morphogenetic processes that produce it;
such knowledge of how organs are made is an essential step in mending
or remaking them.

The idea of the essential similarity of structure of the head and
trunk was early developed by Goethe, who tried to show that the
mammalian skull is a series of modified vertebrae. Unfortunately this

v. 8

PRO-OTIC SOMITES

149

view cannot be maintained in detail and the theory was brought to
ridicule by T. H. Huxley and others. The segmental value of the skull
floor and sides is not at all easy to determine; the parachordals arise
as a pair of unsegmented rods on either side of the notochord.

ma: ha

Fig. 99. Diagram of the segmentation of the head of a dogfish.

cr. limit of neurocranium; vr. limit of visceral arch skeleton; a. auditory nerve; aa.i, pre-
occipital arch; aa.2, occipital arch; ab. abducens nerve; ac. auditory capsule; ah. anterior
head cavity; c. coelom;/. facial nerve; gl. glossopharyngeal nerve; ha. hyoid arch; hm. hypo-
glossal muscles; hy. hypoglossal nerve; la. pila antotica; m. mouth; m.2-6, myomere 2-6;
ma. mandibular arch; tnb. muscle-bud; nc. nasal capsule; om. oculomotor nerve; prf. pro-
fundus nerve; scl. sclerotome of segment 10; sp.1-2, ganglion of spiral nerve 1-2; t. trochlear
nerve; tr. trigeminal nerve; v. vagus nerve; vgl. vestigial ganglion of segment 7; vc. ventral
coelom; vr. ventral root of segment 6. (From Goodrich.)

8. The pro-otic somites and eye-muscles

Ideas about the segmentation of the head were first correctly for-
mulated by F. Balfour. In his studies of the development of elasmo-
branchs (1875) he showed that three myotomes, the pro-otic somites,
can be recognized during development in front of the auditory capsule
(Fig. 99). The auditory sac, pushing inwards and becoming sur-
rounded by cartilage, then breaks the series of myotomes, so that
several are missing in the adult, though the series is complete in the
embryo.

If this analysis is correct we should be able to recognize that the
nerves of the head belong to a series of dorsal and ventral roots,
similar to that in the trunk, the ventral roots being those for the
myotomes and the dorsal roots, running between the myotomes,
carrying sensory fibres for the segment and motor-fibres for any non-
myotomal musculature present (p. 36). In the spinal region the

i5o ORGANIZATION OF THE HEAD v. 8

dorsal and ventral roots join, but this is not the primitive condition
(witness amphioxus and the lampreys), and in the head region the
earlier state of affairs is retained, the dorsal and ventral roots remain
separate. Presumably the arrangement we find in the head today was
laid down in very early times, in the Silurian period or earlier, when
the dorsal and ventral roots were still separate. The head, in spite of
its specializations, preserves for us a relic of that ancient condition.

The branchial nerves, such as the glossopharyngeal, show clear
signs of this condition. Each has a small pre-trematic branch in front
of the slit, a larger post-trematic branch behind it, and a pharyngeal
branch to the wall of the pharynx. The pre-trematic branch usually
contains mostly sensory fibres from the skin, the pharyngeal branch
visceral sensory fibres, including those from taste buds. The post-
trematic branch contains both motor and sensory fibres. In addition
to these more ventral branches the branchial nerves also usually
provide dorsal rami to the skin of the back.

The three pro-otic somites become completely taken up in the
formation of the six extrinsic muscles of the eye, arranged similarly
in all gnathostome vertebrates. The four recti roll the eye straight
upwards, downwards, forwards, or backwards, and the two obliques,
lying farther forward, turn it, as their name suggests, upward or
downward and forward (Fig. ioo). Of these muscles the superior,
anterior, and inferior rectus and inferior oblique are all derived from
the first myotome and are innervated by the oculomotor (third cranial)
nerve. The superior oblique, innervated by the trochlear nerve (fourth
cranial), is the derivative of the second and the posterior rectus
(external rectus of man), innervated by the abducens (sixth cranial),
of the third somite. These three nerves are evidently the ventral roots
of the three pro-otic somites. At some early stage of vertebrate
evolution all the myotomal musculature of the front part of the head
became devoted to the movement of the eyes. The muscles originally
forming part of the swimming series became attached to a cup-like
outgrowth from the brain.

Most of the rest of the musculature of the head, including that of
jaws and branchial arches, is derived from the somatopleure wall of the
coelom and is therefore lateral plate or visceral musculature. This
lateral plate muscle is indeed better developed in the head than in
the trunk, where all the muscles, even of the more ventral parts of the
body, are formed by downward tongues from the myotomes. The
lateral plate origin of the jaw-muscles at once gives us the clue to
the nature of some more of the cranial nerves, the fifth, seventh, ninth,

THE ORBIT

151

and tenth. These nerves all carry ganglia containing the cell bodies
of sensory fibres and these are comparable to the spinal dorsal root

' op prof

olf.b.

cbl sip.

c'd.a.

Fig. 100. Orbit of the dogfish.

ant. reel, anterior rectus; cereb. cerebellum; cil.a., cil.p. anterior and posterior ciliary nerves;
epa. anterior carotid artery; ep. epiphysis; g.cil. ciliary ganglion; inf. obi. inferior oblique;
lam. lamina terminalis of cerebrum; O.V. and VII, superficial ophthalmic branch of trigeminal
and facial; obi. sup. superior oblique; olf.b. olfactory bulb; opt. I. optic lobe; post.rect. posterior
rectus; r. op. prof, ramus ophthalmicus profundus of trigeminal; rs. sensory root of ciliary
ganglion; sup.rect. superior rectus; thai, thalamus; // to A', cranial nerves.
(After Young, Quart. J. Micr. Sci. 75.)

ganglia. But the nerves also transmit motor-fibres to the muscles of
the jaws and branchial arches. They are in fact mixed roots, just as
we have seen that the primitive dorsal roots should be, carrying the
sensory fibres for the segment and motor-fibres for the non-myotomal
muscles (p. 36).

152 ORGANIZATION OF THE HEAD v. 8-

9. The cranial nerves of elasmobranchs

These nerves are more easily studied in elasmobranchs than in any
other vertebrates, because of the relatively soft and transparent
cartilage through which they run. We may therefore take this oppor-
tunity to examine the whole series of cranial nerves in some detail in
the dogfish, beginning with the oculomotor nerve, the first ventral
root. Examination after removal of the brain will show clearly in any
vertebrate, including man, that this nerve arises from the ventral
surface, at the level of the hind end of the midbrain (optic lobes).
This is not true of the trochlear or pathetic nerve, which emerges
from the dorso-lateral surface of the brain but nevertheless is the
ventral root of the second segment. Its cells of origin lie close behind
those of the oculomotor nerve, in the ventral part of the brain. The
reason for the dorsal emergence is that the muscle lies dorsally and the
nerve has been modified so as to reach its muscle by running partly
within the tissues of the brain. The third ventral root (abducens),
which is very short, is clearly ventral.

In looking for the dorsal roots that correspond to these three
segments we have to examine the trigeminal, facial, and auditory
nerves. The trigeminal of the dogfish, like that of man, has ophthalmic,
maxillary, and mandibular branches (Fig. ioo), but can be shown to
represent the dorsal roots of the two first segments. The ophthalmic
branch is a sensory nerve carrying fibres for skin sensation from the
snout. The maxillary branch supplies sensory fibres to the upper jaw,
whereas the mandibular is a mixed nerve to the skin and muscles of
the lower jaw. Besides these main branches there is also a small but
important sensory branch from the trigeminal to the eyeball (Fig.
ioo). This joins a motor root from the oculomotor nerve where the
latter swells slightly to form a ciliary ganglion. Two ciliary nerves
then carry motor and sensory fibres to the eyeball. In some specimens
a branch of the more anterior ciliary nerve leaves the eyeball anteriorly,
runs between the oblique muscles, and out of the orbit again to end
in the skin of the snout (Fig. ioo). Though this branch is small and
inconstant in the dogfish, its course corresponds exactly with that
of a much larger nerve in the related shark Mustelus and in skates and
rays. In these animals there are two ophthalmic branches of the
trigeminal nerve; one, having a course similar to that of the main nerve
in the dogfish, is the ramus ophthalmicus superficialis; the second,
the ramus ophthalmicus profundus, runs across within the orbit, gives
off the long ciliary nerve to the eyeball, passes between the oblique

v. 9 PARTS OF THE TRIGEMINAL 153

muscles, and leaves the orbit for the skin of the snout. In higher
vertebrates the nasociliary nerve and the long ciliary, innervating the
eyeball, represent the profundus, while the rest of the ophthalmic
nerve of mammals corresponds to the superficial ophthalmic of
elasmobranchs.

The relations of these nerves to other structures shows that the
so-called trigeminal nerve really includes the dorsal roots of two
segments combined. The profundus can be traced back in develop-
ment to a nerve that is obviously the dorsal root of the first somite,
of which the oculomotor nerve is the ventral root. Indeed it may be
noticed that the profundus and oculomotor partly join, at the ciliary
ganglion. The ramus ophthalmicus profundus and the oculomotor
nerve thus constitute the dorsal and ventral roots of the first or pre-
mandibular somite, whose corresponding branchial arch is presumably
the trabecula cranii (p. 147). The dorsal root does not show the full
structure of a branchial nerve, presumably because there is no gill-slit.
The profundus represents only the dorsal branch of a typical branchial
nerve, innervating the skin.

The ramus ophthalmicus superficialis, and the maxillary and mandi-
bular branches together constitute the dorsal root of the second pro-
otic somite, whose ventral root is the trochlear nerve. The correspond-
ing gill arch is the mandibular (palato-pterygo-quadrate bar and
Meckel's cartilage), whose gill-slit we have suggested has been in-
corporated with the edge of the mouth. The trigeminal nerve shows
considerable similarity to a branchial nerve, its maxillary branch repre-
sents the pre-trematic and the mandibular the post-trematic ramus,
while the ophthalmicus superficialis is the dorsal branch to the skin.
There is no pharyngeal branch. An anomalous feature of the trige-
minal is that it contains sensory fibres whose cells of origin lie within
the brain (mesencephalic root). These fibres are probably proprio-
ceptors from the masticatory muscles and eye-muscles. The latter run
from the eye-muscle nerves to join the trigeminal.

The dorsal root of the third segment, whose ventral root is the
abducens, includes the whole of the facial and also the auditory nerve.
The facial is a large mixed nerve in the dogfish. Its ophthalmic branch
runs to the snout, carrying mainly fibres for the organs of the lateral
line system that lie there. A large buccal branch supplies sensory
fibres to the mouth and a palatine branch joins the trigeminal. A small
prespiracular branch carries sensory fibres from the skin in front of the
spiracle, and the main portion of the nerve continues behind the
spiracle as the hyomandibular nerve, dividing up into motor branches

i 5 4 ORGANIZATION OF THE HEAD v. 9

for muscles of the hyoid arch and sensory ones for the skin of that
region.

This nerve is obviously the branchial nerve to the spiracle; we can
safely say that the facial and abducens are the dorsal and ventral roots
of the third or hyoid segment. The auditory nerve is included as part
of the dorsal root of the third somite because the auditory sac is
formed by sinking in of a portion of the ectoderm within the territory
of the facial nerve. The labyrinth still communicates with the surface
of the head in the adult dogfish by a canal, the aquaeductus vestibuli.
The nerve that innervates the auditory sac, whatever complexities it
may acquire, is to be regarded morphologically as a portion of the
dorsal root of the hyoid segment.

The segmental nature of the structures in the pro-otic region can
therefore be made out without serious difficulty. The disturbance
introduced by the auditory capsule makes the segmental arrangement
of the more posterior region of the head somewhat confused. The
series of dorsal roots is uninterrupted; the ninth (glossopharyngeal)
nerve is the dorsal root of the fourth segment of the series and runs
out through the cartilage of the auditory capsule. The dorsal roots of
the succeeding segments are then fused to form that very puzzling
nerve the vagus. The branches it sends to the gills are clearly typical
branchial nerves, but why should they all come off together from the
medulla oblongata, and if there is any advantage in this union, why
is the ninth nerve not also so incorporated? Above all, why does
the vagus send two branches far outside the segments of its origin, the
lateral line branch carrying fibres to the organs right to the tip of the
tail and the visceral branch fibres to the heart, stomach, and probably
small intestine?

Evidently these 'wanderings', from which the vagus gets its name,
began very long ago. The nerve reaches as far back in cyclostomes as
in any other vertebrates. It is easy to understand that if visceral
functions are to be directed from the medulla oblongata there is an
advantage in having sensory impulses sent direct to that region of the
brain and motor impulses sent out direct to the viscera. It may be
that these advantages allowed the centralization of these visceral
functions, while the need for serial contraction of the swimming
muscles led to the retention of the segmental arrangement of the
spinal cord. It is an interesting thought that but for the swimming
habits of our ancestors our nervous system might by now consist of a
central ganglion with nerves passing from it direct to all the organs.
Indeed we are tending in that direction, as the spinal cord shortens

v. 9 VAGUS NERVE 155

and becomes more and more nearly a simple pathway between the
brain and the periphery.

However this may be, the vagus is certainly a nerve compounded
of the dorsal roots of several segments and it is a mixed nerve, con-
taining both receptor and motor fibres. Some of the more posterior
rootlets of this series are separated off in higher animals (not the dog-
fish) to form the eleventh cranial nerve, the accessorius or spinal
accessory, which in mammals sends motor-fibres to certain muscles
of the neck, the sternomastoid, and part of the trapezius. Its motor
nature has led some to suppose that this nerve is a ventral root, but
these muscles are derived from lateral plate musculature and the
accessorius represents the motor portion of the hinder dorsal roots
of the vagus series.

The ventral roots of this post-otic region have become much
reduced. Several myotomes are always missing completely, so that
there are no ventral roots corresponding to the glossopharyngeal and
first three or four vagal segments. The more anterior of the surviving
post-otic somites are to be found not in the dorsal region but ventrally,
as the hypoglossal musculature of the tongue. The muscle-buds have
grown round into this portion behind the gill-slits, and the nerve
(hypoglossal) that innervates them represents the ventral roots of the
more posterior segments of the vagus-accessorius series (Fig. 104).
The origin of this nerve from the floor of the medulla is a clear sign
that it is a ventral root.

Thus the entire series of cranial nerves is :

Segment

Arch

Dorsal root

Ventral root

Pre-mandibular

Trabecula

R. op. profundus V

Oculomotorius III

Mandibular

Palato - pterygo - quad-

Rr. op. superficialis,

Trochlearis IV

rate bar and Meckel's

maxillaris, and man-

cartilage

dibularis V

Hyoid

Facialis VII
Acousticus VIII

Abduccns VI

1st Branchial

1 st Branchial

Glossopharyngeus IX

(absent)

2nd Branchial

2nd Branchial^

Vagus X

3rd Branchial

3rd Branchial 1

Hypoglossals XII

4th Branchial

4th Branchial j

Accessorius XI

5th Branchial

5th Branchial J

Two cranial nerves have not yet been considered, the first, olfactory,
and second, optic. Our thesis is that all connexions between centre
and periphery are made by means of a segmental series of dorsal and
ventral roots and therefore these nerves, too, should be fitted into the
series. No embryological or other studies have enabled this to be done

156 ORGANIZATION OF THE HEAD v. 9-

and the reason in the case of the optic nerve is quite clear. It is not
morphologically a peripheral nerve at all. The eye is formed as a
vesicle attached to the brain ; the optic 'nerve' therefore develops as a
bundle of fibres joining two portions of the central nervous system; in
fact it is now usually called the optic tract, not the optic nerve.

This reasoning will not apply to that very peculiar and interesting
structure the olfactory nerve. This is unique among all craniate
nerves in consisting of bundles of fibres whose cell bodies lie at the
periphery. The cells of the olfactory epithelium, like the sensory cells
in invertebrates and some of those of amphioxus, are neurosensory
cells, that is to say, their inner ends are prolonged to make the actual
nerve-fibres that pass into the brain. This fact does not by itself solve
the problem of fitting the nerve into the series of dorsal and ventral
roots, but it reminds us that the nerve is very ancient, and suggests
that it does not fall into the rhythm of the rest of the series because it
precedes the other cranial nerves either in time or space, or perhaps
even both. The olfactory nerve may have existed before any seg-
mental structure appeared, possibly as the nerve of sense-organs on
the front end of the ciliated larva which we suppose gave rise to our
stock (p. 76). Alternatively we can say that the olfactory nerve is as
it is because it lies in front of the region over which the segmenting
process operates; it is, as it were, 'prostomial'. If we wish we can hold
both these views together.

There are one or two other exceptions to the rhythmic arrangement
of nerves, perhaps more difficult to account for than the first and
second cranial nerves. If all connexions between centre and periphery
are made by dorsal and ventral roots what is the status of the fibres
that run down the infundibular stalk to reach the cells of the pituitary
body? This glandular tissue, derived from the epithelium of the
hypophysial folding of the roof of the mouth, is undoubtedly a peri-
pheral organ. Does it receive its nerve-fibres direct from the brain ?
If so presumably we must say that the pituitary, like' the nose,
is prostomial, lying in front of the segmental region, and this is
reasonable enough from its position. There is good reason to believe
that it is an extremely ancient organ, already present in the earliest
chordates.

A still more puzzling exception is the nervus terminalis. This is
a small bundle leaving the brain ventrally behind and below the olfac-
tory nerves and running to the olfactory mucosa or to the accessory
olfactory organ of Jacobson, where this is present (p. 350). In some
vertebrates it carries a small ganglion. The fibres are probably

v. io RESPIRATION 157

afferents and they run backwards through the brain tissue to the
pre-optic nucleus of the hypothalamus. A possible clue to its origin is
that this is the region of the brain where the morphologically ventral
region of the neuraxis ends (p. 147). The nervus terminalis may repre-
sent the ventral olfactory nerve, the much larger main nerve being
morphologically dorsal.

A further puzzle of some importance which may be mentioned here
is the course of the proprioceptor fibres for those muscles that are
supplied purely by ventral roots. The eye-muscles contain proprio-
ceptor organs and Sherrington and others have shown that the affer-
ent fibres connected with these run to the brain through the third,
fourth, and sixth nerves, that is to say, through ventral roots. Simi-
larly, it has been shown that there are afferent fibres in the hypo-
glossal nerves in mammals. Conversely it is now known that there are
efferent fibres running from the brain to many receptor organs. For
example, such fibres run in the auditory nerve. To pursue these ques
tions farther would lead us into discussion of the factors that control
the making of connexions within the nervous system Here we are
concerned only with analysis of the plan that produces the main out-
lines of the structures in the head, a plan which, with all its modifica-
tions, is essentially segmental.

10. Respiration

The function of the branchial arches is not merely to support the
gills but to allow the movements of the pharynx wall by which the
respiratory current of water is produced. It is for this reason that
the jointed system of rods is present. The respiratory movements con-
sist in a lowering of the floor of the mouth by means of the hypo-
glossal muscles, with at the same time an expansion of the walls of
the pharynx. This causes an inrush of water through the mouth,
which is then closed and the floor raised, forcing the water out through
the gill-slits. The whole movement is worked by the 'visceral' (lateral
plate) muscles of the pharynx wall, innervated by the trigeminal,
facial, glossopharyngeal, and vagus nerves, in co-operation with the
myotomal hypoglossal muscles, innervated by the hypoglossal nerve.

The gill filaments bear lamellae that meet at the tips, leaving minute
channels for the water. The blood flows through the lamellae in the
opposite direction to the water so that just before leaving the gills
the blood meets the highest concentration of oxygen and lowest of
carbonic acid.

158

ORGANIZATION OF THE HEAD

1 1 . The gut of elasmobranchs

The digestive system of sharks shows several changes from the plan
found in lampreys, especially the presence of a true stomach, charac-
teristic of all gnathostomes. Apparently little or no digestion goes on
in the mouth and pharynx. The teeth consist of rows of backwardly
directed denticles (Fig. ioi). They are carried on special folds of skin
lining the jaws and are continually replaced as they are worn away on

Fig. ioi. Sections through the jaws of a, dogfish (Scyliorhinus), and n, sand-shark

(Odontaspis), showing the transitions between dermal denticles (d) and teeth (t).

(From Norman, partly after Gegenbaur.)

the edge. The replacement of milk by permanent teeth in mammals
is a relic of such serial replacement in a fish. The 'gill rakers' arc
rods attached to the branchial cartilages and serving to prevent
the escape of prey. The basihyal supports a short non-protrusible
tongue.

The wall of the pharynx is lined by a stratified epithelium on to
which open numerous mucous glands, sometimes complex. The mucus
serves to assist the passage of the food, but probably has no strictly
digestive function, though the salivary glands of higher vertebrates
no doubt originate from a modification of these mucous glands.

The pharynx narrows to an oesophagus with thick muscular walls,
leading without sharp transition to the stomach. We have seen that in
cyclostomes the oesophagus opens directly into the region of gut that
receives the bile and pancreatic secretion. The stomach, which we

v. 12 DIGESTION IN ELASMOBRANCHS 159

now meet for the first time, has probably been formed as a special
portion of the oesophagus. Barrington suggests that it evolved with the
jaws, serving originally as a receptacle for the large pieces of food, or
even whole fishes, which could now be swallowed. The mucous glands
became modified to produce acid, since this prevents bacterial decay.
Finally, an enzyme, pepsin, was evolved able to digest proteins in
acid solution. In the dogfish this condition has been fully established
and the stomach has essentially the structure and functions found in
all higher vertebrates. However, in the gastric glands only one type
of cell is recognizable, there are no separate pepsin-secreting and
acid-producing cells. Nevertheless, there is a pepsin-like enzyme
present and the contents are acid. The stomach is divided into two
parts, a descending cardiac and ascending pyloric limb, the signifi-
cance of the divisions being unknown.

The region where the stomach joins the intestine is guarded by a
powerful pyloric sphincter, immediately beyond which open the bile
and pancreatic ducts. The liver is a large two-lobed organ, receiving
the hepatic portal blood from the gut. It serves as a storage organ
containing much glycogen and fat and sometimes the hydrocarbon
squalene. It probably also plays a part in the destruction of red blood
corpuscles. Bile is carried away to a gall-bladder, from which a bile-
duct leads to open at the front end of the spiral intestine.

The pancreas, hardly recognizable as a distinct organ in the lamprey,
forms in the dogfish an elongated body between the stomach and
intestine. It contains both exocrine and endocrine cells and its duct
enters the intestine shortly below the pylorus. The 'small' intestine
of elasmobranchs is of a peculiar form, being short but with its
surface greatly increased by the presence of a spiral ridge or 'valve'.
The intestinal contents are alkaline and contain trypsin, amylase,
and lipase. There is no constant fauna of commensal bacteria. Ab-
sorption presumably takes place wholly in this organ, for the remain-
ing length of gut consists only of a short rectum, to which is attached
an organ of unknown function, the rectal gland, containing branched
glands and much lymphoid tissue.

12. The circulatory system

The heart develops as a specialization of the subintestinal vessel
between the place where it receives the veins from the liver and the
body wall and the gills, which are to be supplied under high pressure.
It consists of a single series of three main chambers, sinus venosus,

i6o

ORGANIZATION OF THE HEAD

atrium, and ventricle, all of which are muscular, and there is also a
muscular base to the ventral aorta, the conus arteriosus, provided with
valves (Fig. 102).

The five afferent branchial arteries carry blood to the gill lamellae,
whence it is collected by a system of four efferents and connecting
vessels into a median dorsal aorta, carrying blood to all parts of the
body. Oxygenated blood is supplied to the head from three sources.
(1) From the top of the first gill a carotid artery leaves the efferent
branchial and runs forwards and towards the midline: it then divides

f. eF pef

Fig. 102. Diagram of the branchial circulation of an elasmobranch fish.

aa. median anterior prolongation of aorta; ac. anterior carotid; afa. afferent vessel of spiracu-
lar gill; aef. afferent vessel from last hemibranch; af. anterior efferent vessel; a/. 2-6 , five
afferent vessels from ventral aorta; afa. afferent artery of spiracular gill; c. conus leading to
ventral aorta; cl. coeliac artery; d. ductus Cuvieri; da. dorsal aorta; ef. epibranchial artery;
h. a. hyoid afferent vessel; hp. hepatic veins; ht. heart; pc. posterior carotid; pef. posterior

efferent vessel; s. spiracle; va. ventral artery; I-V, branchial slits.

(From Goodrich, Vertebrata, A. & C. Black, Ltd., after Parker.)

into an external carotid to the upper jaw and internal carotid to the
brain. (2) The dorsal aorta divides at its front end into branches,
which join the carotids before their division. (3) From the vessel
that collects blood from the first gill arises a hyoidean artery, carry-
ing oxygenated blood to the spiracle. From here the hyoidean artery
runs on as the anterior carotid (Fig. 102) across the floor of the orbit
to join the internal carotid within the brain-case.

The heart is supplied by a cardiac artery arising from the dorsal
aorta behind the gills. The blood-pressure in the ventral aorta is 30-40
mm Hg and there is a drop of 10-20 mm Hg across the gills. The
circulation is slow, with a mean circulation time as low as 2 minutes.
The venous return of the fishes is ensured by a system of very large
sinuses. The pericardium is almost completely enclosed in a carti-
laginous framework by the basibranchial plate above and pectoral
girdle below it. It may be that this produces a negative pressure in

v. iz VASCULAR SYSTEM OF ELASMOBRANCHS 161

the veins. There is a passage of unknown function, the pericardio-
peritoneal canal, leading from the pericardium to the abdominal
coelom and the hinder end of this is very narrow.

A caudal sinus from the tail opens into a renal portal system above
the kidneys. From the latter, and from the muscles of the back, blood is
collected into the pair of very large posterior cardinal sinuses, lying on
the dorsal wall of the coelom. Above the heart these receive the open-
ings of other large sinuses, such as the anterior cardinal sinus, running
above the gills and collecting blood from the head by way of an orbital
sinus, and the jugular, lateral cardinal, subclavian, and other sinuses from
the body wall. Blood then passes round the oesophagus in the two
ductus Cuvieri into the sinus venosus, where hepatic sinuses also open.

The resistance offered by a vessel to flow within it decreases with
approximately the fourth power of the diameter, therefore the large
size of these vessels substantially assists in allowing return to the
heart. The heart-muscles, like any others, require antagonists; they
can contract in one direction only, and each chamber therefore needs
to be actively dilated. It will be noted that the fish heart consists of
a series of three muscular chambers, presumably because the low
venous pressure is able to dilate only a chamber with very thin walls,
such as the sinus venosus. Contraction of the sinus then inflates the
auricle, and the auricle inflates the ventricle, which thus constitutes
the third step in this serial pressure-raising system. In the land animals,
where most of the blood only passes through a single set of capillaries,
a two-step system (auricle and ventricle) is sufficient for each part of
the circulation.

Little is known of the control of the circulation but it is probably
less effective than in higher animals. There is a cardiac branch from
the vagus ending in an elaborate plexus in the sinus venosus (Fig. 104).
Stimulation of this nerve slows the heart. There is no anatomical or
physiological evidence of a sympathetic nerve to the heart, but
abundant sympathetic fibres run to the arteries. Small doses of adren-
aline cause prolonged rise of blood-pressure.

There are receptors in the efferent branchial vessels and in the post-
branchial plexus above the cardinal veins (p. 175). Nerve impulses
from these receptors can be recorded in the vagus at each systole and
are increased by raising the blood-pressure. Their reflex effects are
to slow the heart and respiration and decrease the blood-pressure,
perhaps for protection of the gill capillaries. These reflexes are pre-
sumably the ancestors of the carotid sinus and similar reflexes of land
vertebrates.

162 ORGANIZATION OF THE HEAD v. 13

13. Urinogenital system

The blood of the elasmobranchs differs from that of all other verte-
brates in its very high content of urea. As measured by the depression
of the freezing-point the blood is isotonic with the surrounding sea
water (say, 3-5 per cent. NaCl); it may even be slightly hypertonic.
But there is far less salt in the blood than in the sea, in fact only
about 1-7 per cent. NaCl. Although the blood is nearly isotonic with
the sea its composition is therefore regulated (homeosmotic). This
arrangement is apparently a legacy of the fact that the ancestors of the
elasmobranchs were originally fresh- water animals (p. 187). The
return passage to the sea has been accomplished by the elasmobranchs
through the device of urea retention. The gill surfaces, in which alone
the blood comes into close contact with sea water, are not permeable
to urea, but this substance penetrates freely into the tissues, as it does
in other animals. Elasmobranch tissues if placed in sea water are
therefore in contact with a strongly hypertonic medium. They are so
habituated to the presence of urea that they are unable to function
unless it is present in a concentration that would be toxic to most
animals.

This arrangement has presumably been responsible for the fact
that few of the elasmobranchs have returned to fresh water. In the
case of the saw-fish Pristis, which lives some hundreds of miles
up the Mississippi and various rivers in China, Smith found that a
considerable concentration of urea is still maintained in the blood,
thus further increasing the work that these fishes, like any fresh-water
animal, must do in order to maintain an osmotic concentration above
that of the surrounding water. One shark (Carcharhinus nicaraguensis)
and some rays, Trygon, also live in fresh water.

In the ordinary marine elasmobranchs the high urea concentration
is maintained by the presence of a special urea-absorbing section of
the kidney tubules. The urinary apparatus is a mesonephros and
these fishes show a considerable specialization in that the urinary
functions of this organ are separated from its generative ones in the
male. The hinder part of the kidney (sometimes called opisthone-
phros, the term metanephros should be used only for the definitive
kidney of amniotes, which has a different method of development)
consists of a mass of tubules ending in very large glomeruli, and a
section of each tubule has the function of urea absorption. All the
tubules join to form a series of five urinary ducts and these enter a
urinary sinus, opening to the cloaca. The sinus can be compared

v. 13 URINOGENITALS OF ELASMOBRANCHS 163

functionally with a bladder, but it is a mesodermal structure, derived
from the main kidney duct, and not strictly comparable to the endo-
dermal bladder of tetrapods. The urinary sinus is a small organ and
the volume of liquid excreted is small.

Fie. 103. A. Urinogenital system of the female, B, of the male dogfish.
ah.p. abdominal pores; cl. cloaca; cp. claspers of the male; F. rudiment of the oviducal opening
in the male; Md. urinary ducts; mtn. hinder (excretory) part of mesonephros; od. oviduct;
oe. cut end of oesophagus; of. oviducal funnel; og. oviducal gland; ov. ovary; P.f. pelvic fins;
R. rectum; s.s. sperm-sacs; T. testis; up. urinary papilla in the female; ugp. urogenital papilla
in the male; vs. urinary sinus; vc. vasa efferentia; vs. vesicula seminalis; WD. Wolffian duct;
Wg. Wolffian gland or mesonephros. (After Bourne, from Goodrich, Vertebrata, A. & C.

Black, Ltd.)

The genital system is highly specialized to allow internal fertiliza-
tion and the production of a few very yolkv and well-protected eggs.
There is a single large ovary, from which the eggs are carried by the
cilia of the peritoneum to a pair of funnels lying on either side of the
liver behind the heart (Fig. 103). These are apparently formed from
proncphric funnels and the Mullerian duct (oviduct) separates from
the original nephric duct. In the adult it becomes a thick-walled
muscular tube, bearing a swelling, the nidamental gland, the upper
part of which produces albumen, the lower the horny egg case.

1 64 ORGANIZATION OF THE HEAD v. 13-

The testes are paired and sperms are collected at their front ends
by vasa efferentia leading into the anterior or reproductive portion of
the mesonephros. This consists of a much coiled, thick-walled, vas
deferens, whose glands produce material that aggregates the sperms
into spermatophores. The vas expands into a broader ampulla
(seminal vesicle), which at its lower end gives off a forwardly directed
blind diverticulum, the sperm sac, developmentally the lower end of
the Miillerian duct, reduced of course in the male; small funnels are
still visible at the upper end.

Transmission of the sperms is produced by a large and complicated
pair of claspers. These are modified parts of the pelvic fins of the
male, developed into scroll-like organs and containing a pumping
mechanism and erectile tissue; they are inserted into the female
cloaca. The mechanism of erection is operated by nerves and may
involve the liberation of adrenaline; experimental injection of that
substance will produce erection, and it is perhaps significant that the
male possesses a reserve of adrenaline-producing tissue (see p. 167).

Development of elasmobranchs is by partial cleavage, producing a
blastoderm, perched on the top of a large mass of yolk. The egg is
protected by an elaborate egg-case, the 'mermaid's purse', within
which development proceeds until the yolk has been used up.

In several elasmobranchs development is viviparous, the oviduct
forming a 'uterus'. In Mustelus there is a yolk-sac placenta, but in
Trygon 'uterine milk' is secreted into the embryo by villi (trophone-
mata) inserted through the spiracles.

14. Endocrine glands of elasmobranchs

Elasmobranch fishes possess the full complement of endocrine
glands, but these show some interesting differences from those of
higher vertebrates. The pituitary body lies in the usual place below
the diencephalon and anterior, intermediate, tuberal, and neural
divisions can be recognized. Little is known of the functions of the
gland. The gonads of the dogfish retrogress after removal of the pitui-
tary. Little or no vasopressin or oxytocin is present. The neuro-
intermediate lobe contains a substance that produces the expansion
of melanophores. Hogben and Waring have also produced evidence
that the pars anterior produces a substance causing contraction of the
melanophores, but this has not yet been isolated and the evidence for
its existence is indirect.

The thyroid is formed by a downgrowth from the floor of the
pharynx, to which it often remains attached by a narrow stalk con-

v. i 4

ADRENAL TISSUE

165

sp n

Fig. 104. Dissection of suprarenal bodies and sympathetic nervous system of the

dogfish.
b.a. brachial artery; c.a. coeliac artery; d.a. dorsal aorta; g. first sympathetic ganglion; hyp.
hypoglossal nerve; I.e. longitudinal sympathetic 'chain'; n.card. cardiac branch of vagus;
p.b.p. post-branchial plexus; r.c. ramus communicans; s. sensory fibre; s.a. segmental artery;
sg. sympathetic ganglion; sp.a. anterior splanchnic nerve; sp.m. middle splanchnic nerve;
spa. spinal nerve; sup. suprarenal body; v. ventricle; v.d. vas deferens; vs. vago-sympathetic
anastomosis; X. vagus; X.br. branchial branch of vagus; X.visc. visceral branch of vagus.
(After Young, Quart. J. Micr. Sci. 75.)

taining a small ciliated pit, a reminder that the organ was once a
ciliated mucus-secreting gland.

The adrenal tissue is especially interesting because the two parts,
so closely associated in mammals, are here found widely separated. A
segmental series of glands, the suprarenals, are rich in noradrenaline.
They project into the dorsal wall of the posterior cardinal sinus and can
be seen when it is opened (Fig. 104). The more anterior ones are
fused to form an elongated structure on either side of the oesophagus.

(i 66)

n v

Fig. 105. Diagram of transverse section through hind region of mesonephros of

dogfish.

cv. cardinal vein; da. dorsal aorta; int. interrenal body; k. mesonephros; I c. longitudinal

sympathetic connective; n c. sympathetic nerve-cells scattered in suprarenal body; nv.

sympathetic nerves; re. ramus communicans; sg. sympathetic ganglion; sv. subcardinal vein;

sup. suprarenal body. (From Young, Quart. J. Micr. Sci. 75.)

Fig. 106. Diagram of arrangement in hinder mesonephric region of dogfish.
Lettering as Fig. 105. tr. transverse sympathetic nerve. (From Young, Quart. J. Micr. Sci. 75.)

v. i 4 -i5 BRAIN OF ELASMOBRANCHS 167

The sympathetic ganglia are closely associated with these suprarenal
bodies, as would be expected from their common origin from cells
of the neural crest. The segmental series continues along the whole
length of the abdomen, the more posterior members being embedded
in the kidney tissue (Fig. 105). These posterior suprarenal bodies are
larger in the male than in the female, but only the central part of the
male glands shows the reaction with chrome salts that indicates the
presence of adrenaline. The peripheral portion of each gland appears
to consist of non-functioning cells, possibly a reserve used only during
reproduction (see p. 164).

The part of the adrenal corresponding to the cortex of mammals is
represented in elasmobranchs by the interrenal bodies, lying medially
in some species, paired in others, in the kidney region (Figs. 105 and
106). The cells of these organs resemble cortical adrenal cells. Since
they are not in contact with the suprarenals at any point, it would seem
that the association of the two parts is not necessary for their function-
ing, at least in these animals. Removal of the interrenal is always fatal.
The gland is stimulated by 'stress' or by mammalian ACTH. Extracts
of it prolong the life of adrenalectomized rats. There is evidence that
it influences carbohydrate metabolism and activity of the gonads but
not electrolyte balance.

The islets of Langerhans contain two cell types as in mammals.
The pineal body is small and without any trace of eye-like structure.

The gonads contain endocrine organs, producing steroid hormones.
These are formed by interstitial cells in the testes. Oestrogens probably
come from the outer (theca) cells of the follicles that surround the
eggs. The inner (granulosa) cells of the capsule assist in yolk produc-
tion but may also produce progesterone and in viviparous species
they develop into a distinct corpus luteum after ovulation.

15. Nervous system

The brain is large and well developed in elasmobranchs, having a
structure characteristically different from that of both the cyclostomes
and bony fishes (Fig. 100). The forebrain is large and has cerebral
hemispheres thickened both in floor and roof, whereas in teleosts the
roof is thin. The hemispheres are wide relative to their length and the
end of the unpaired portion of the forebrain between the hemispheres,
the lamina terminalis, is also much thickened. Attached to the ends
of the cerebral hemispheres are large olfactory bulbs and there are
also large nasal sacs. Evidently the olfactory sense is well developed
in these animals and they depend greatly on it for hunting.

1 68

ORGANIZATION OF THE HEAD

v. 15

All parts of the cerbral hemispheres receive fibres from the olfac-
tory bulbs and the forebrain serves mainly for analysing the olfactory
impulses. However, it is stated that there are fibres reaching forward
to one area at the back of the roof of the hemispheres from other
centres. Johnston therefore called this region the 'general somatic
area' and suggested that it represents the beginnings of that develop-
ment so characteristic of mammals by which all the senses are centred
on the cerebral hemispheres. Further work is needed to confirm the

Dec interhemisph

., Tr medianus

Ventr o/f

Tr olFacb.

Tr olFacb. epistr cruc.

Fiss Urn tel.

Ventrical, /at.

Fig. 107. A cross-section through the forebrain of a shark.

Dec. interhemisph. decussatio interhemispherica; Fiss.lim.tel. fissura limitans telencephali;

Prim. hip. primordium hippocampi; 5. septum; Striat. striatum; Tr. medianus. tractus

medianus; Tr.oljact. tractus olfactorius; Tr.olf act. epistr. cruc. tractus olfacto-epistriaticus

cruciatus; Ventricul.lat. ventriculus lateralis; Ventr. o.f. ventriculus olfactorius.

(From Kappers, Huber, and Crosby.)

existence of this pathway, and even if present its significance must
not be exaggerated. There is of course no cortical arrangement of
tissue in the hemispheres. The cells form thick masses around the
ventricle (Fig. 107). The roof is quite thick and contains decussating
fibres in the midline. The sides and floor make up the main bulk of the
organ, the lateral wall being known as the striatum, its upper part the
epistriatum. The medial wall is known as the septum and its upper
portion is often referred to as the primordium hippocampi, having a
position similar to that of the hippocampus of mammals. The main
efferent pathways are tracts leading to the hypothalamus and to the
optic lobes. After removal of the forebrain the sense of smell is lost
but the fish shows no obvious disturbance of posture, locomotion, or
behaviour.

The diencephalon is a narrow band of tissue, there are no extensive
tracts leading forward through it, and the optic and other pathways
do not end here as they do in higher animals. The lower part of the

v. 15 BRAIN OF ELASMOBRANCHS 169

between-brain, the hypothalamus, is, however, as well developed
(relatively) in these animals as in mammals. Its hind part (inferior
lobes) receives olfactory impulses via the forebrain (the 'fornix' of
higher vertebrates) and gustatory pathways from the medulla. Its
efferent fibres run to reticular centres. The more anterior part of the
hypothalamus lies above the pituitary and contains the supraoptic
nucleus, whose axons form the hypophysial tract, ending in the inter-
mediate lobe. The supraoptic cells of all vertebrates are large and
contain granules of neurosecretory material that is probably passed
down the axons and liberated in the pituitary. The anterior hypo-
thalamus is a higher centre for visceral control, regulating, for
example, circulation, respiration, and many metabolic activities.
Attached to the hind end of the hypothalamus of fishes is a peculiar
organ, the saccus vasculosus, with folded, pigmented walls. It has
been suggested that this acts as a pressure receptor, since it is well
developed in deep-sea fishes. It is one of the characteristic features
that the sharks and bony fishes have in common.

The midbrain, as in cyclostomes and teleosteans, is very large and is
perhaps the dominant centre of the brain. The optic tracts end in its
roof (tectum opticum) after complete decussation below the brain.
The cells of the tectum are arranged in a complicated pattern of
layers. Other sensory centres that send tracts to the optic lobes are
the olfactory (cerebral hemispheres), acustico-lateral, cerebellar,
gustatory, and probably also the general cutaneous centres of the
spinal cord. Efferent tracts leave the midbrain roof to the base of
the midbrain and extend backwards into the medulla, perhaps into the
spinal cord. The efferent midbrain fibres have direct influence on
the spinal cord, and electrical stimulation of points on the tectum
opticum produces various movements of the fins, suggesting a system
of control similar to that exercised over spinal centres by the cerebral
cortex of mammals through the pyramidal tract. Various forced
movements follow injury to the midbrain.

The cerebellum is a very large organ in clasmobranchs, as in all
animals that move freely in space. Its main source of sensory fibres is
from the ear and from the organs of the lateral line system, whose
afferent fibres enter through the seventh, ninth, and tenth cranial
nerves. The internal structure of the cerebellum is very uniform and
essentially similar in all vertebrates. Removal of portions of it from
dogfishes produces aberrations of swimming.

The medulla oblongata is the region from which most of the cranial
nerves spring and especially those that regulate the respiration and

i7o ORGANIZATION OF THE HEAD v. 15-

visceral functions. In mammals this control is indirect, but in fishes
the nerves that spring from the medulla directly innervate the
respiratory muscles of the gills and floor of the mouth. It is no doubt
for this reason that the centre for the initiation of the respiratory
rhythm developed in the medulla.

16. Receptor-organs of elasmobranchs

The paired nasal sacs have much-folded walls. Water enters by a
single opening but this may be partly divided by a fold, making a
groove, which may open to the mouth. There are taste-buds scattered
over the wall of the pharynx. It has been shown experimentally that,
as in higher animals, these are receptors for sampling the food after
it has been brought close to the animal, whereas the nose acts as a
distance receptor. Smell and taste are therefore different senses for a
dogfish, as for us. By training fishes to discriminate between various
substances it can be shown that those that we should smell are
detected by the nose in the dogfish, but its organs of taste, like ours,
can discriminate only between a few qualities, including salt, sour,
and bitter.

The eyes are well developed in sharks and no doubt serve as an
important means of finding the prey and avoiding enemies. However,
the retina usually contains only rods, and visual discrimination is
probably poor, but there are cones in Mustelus and Myliobatis. Unfor-
tunately details as to the functional performance of the eyes, ability to
discriminate shapes, &c, are scanty. Behind the retina there is often a
reflecting layer, the tapetum lucidum. This may be provided with
pigment cells, which expand in the light but contract in darkness,
allowing the underlying guanophores to reflect, thus increasing
sensitivity. The lens is spherical and very hard, as in all fishes, since
it must perform the whole work of refraction. It is provided with a
protractor-lentis muscle, presumed to produce active accommodation
for near vision by swinging the lens forward. The iris is peculiar in
those elasmobranchs that hunt by day; when it narrows it divides
the pupil into two slits by the descent of an upper flap or operculum.
The muscles of the iris are better developed in elasmobranchs than
in most bony fishes and the pupil makes wide excursions. The
sphincter iridis muscle, which narrows the pupil, works as an inde-
pendent effector. It is stimulated to contract by light, but its move-
ments are not controlled by any nervous mechanism. The radial
dilatator fibres, which open the pupil, receive motor-fibres from the
oculomotor nerve. The closure of the iris when illuminated is

v. i6 RECEPTORS OF ELASMOBRANCHS 171

relatively slow. If the whole eye is cut out from the head, in the dark,
the sphincter, being an independent effector, still closes when illumi-
nated. The muscle, being without nerves, is not affected by any of the
usual drugs that mimic action of the autonomic nervous system,
though some of these affect the innervated dilatator muscle. We have
therefore the curious situation that no 'autonomic' drugs applied to
the isolated dark adapted eye cause closure of the pupil ; this can only
be produced by illumination (Fig. 108).

The ear of elasmobranchs contains receptors concerned (1) with
maintenance of muscle tone, (2) with angular accelerations, (3) with

Red

White

Adrenaline j//00,000

Minutes

Fig. 108. Movements of margin of pupil of an isolated iris of the shark Mustelus,
followed by plotting with a camera lucida and here shown magnified 53 X . Addition
of adrenaline causes slight dilation of the already dilated pupil and illumination then
causes closure. Acetyl choline even in concentrations of 1 in 10,000 has a similar
dilatory effect. (From Young, Proc. Roy. Soc. B. 112.)

gravity, (4) perhaps with hearing. There are three pairs of semi-
circular canals, each with an ampulla containing receptor cells, whose
hairs are embedded in a gelatinous cupula. This behaves as a highly
damped torsion pendulum, swinging with movement of the fluid.
These receptors discharge impulses continuously and during angular
rotations the frequency is either increased or decreased in the appro-
priate ampullae, initiating compensatory movements of the eyes and
fins.

The otolith organs include three patches of receptor cells in par-
tially distinct sacs, the utricle, saccule, and lagena. The endolym-
phatic duct is an open canal and in some species serves to admit sand
grains, which are attached to the maculae as gravity receptors. The
utricle seems to be the main receptor producing appropriate postures
in relation to gravity. The lagena shows a maximum discharge rate
near the normal position of the head and thus serves as an 'into level'
receptor. The areas of these maculae that carry otoliths do not
respond to vibrational stimuli but carry only gravitational receptors.
Vibration responses in the form of nerve impulses have been seen
in rays but only up to 120 c/sec, although vestibular microphonics
up to 750 c/sec occur. At high intensity there is much synchronization

172 ORGANIZATION OF THE HEAD v. 16-

of units. These results suggest that the ear may function as a vibration
receptor, but there are no conditioning experiments to show whether
these fishes can hear.

There is a well-developed system of lateral line organs, whose
function is considered later (p. 218). The organs of this system on the
head are highly modified in elasmobranchs to form the ampullae of
Lorenzini, long canals filled with mucus. Sand showed that these

Fig. 109. Drawing of a sympathetic ganglion and related structures in a dogfish.
Lettering as in Figs. 104 and 105. s.o. sense-organs. (After Young, Quart. J. Alter. Sci. 75.)

organs increase their discharge of nerve impulses with very slight
falls of temperature, and he suggested that their function is to detect
such changes. They are also sensitive to weak tactile stimulation and to
small voltage gradients in the water. Their function therefore remains
uncertain. It may be related to determining changes of hydrodynamic
pressure distribution over the surface of the aerofoil-like body,
especially in skates and rays. They may thus act as mechano-receptors
detecting local changes of pressure near the body surface.

No doubt elasmobranchs, like other animals, have many senses
referred to the skin, such as we call touch, pain, and the like, but few
studies of these exist. Sand has shown the presence of volleys of
impulses in the nerves connected with muscles when the latter are
stretched. Proprioceptors have been demonstrated histologically in
the muscles of Raja. This agrees with the fact that after severance of
the spinal cord the swimming rhythm only continues if some afferent
nerves are intact.

v. 17

SYMPATHETIC OF ELASMOBRANCHS

173

17. Autonomic nervous system

The sympathetic system of elasmobranchs consists of an irregular
series of ganglia, approximately segmental, lying dorsal to the pos-
terior cardinal sinus and ex-
tending back above the kidneys.
These ganglia contain motor
nerve-cells (post - ganglionic
cells) whose ascons end in the
smooth muscles either of the
arterial walls or of the viscera.
The cells themselves are con-
trolled by pre-ganglionic nerve-
fibres whose cell bodies lie in
the spinal cord and whose pro-
cesses run out in the ventral
spinal roots and rami com-
municantes (Fig. 109). In
higher animals the sympa-
thetic ganglia send postgangli-
onic fibres back to the spinal
nerves for distribution to the
skin ('grey rami communi-
cantes') but these are absent in
elasmobranchs and correspon-
dingly there is no evidence of
sympathetic control of skin
functions (e.g. chromato-
phores); a very different con-
dition is found in bony fishes
(p. 222). Another peculiarity
of the sympathetic system of
elasmobranchs is that it does
not extend into the head. This
condition is unique among
vertebrates, but it is not clear
whether it is primary or the
result of a secondary loss.

In mammals it is usual to
recognize a parasympathetic
system acting in antagonism to

symp

Fig. i 10. Diagram of the autonomic nervous

system of the dogfish.
art. artery; card.n. cardiac nerve; cil.g. ciliary gang-
lion; ft. heart; in. intestine; k. mesonephros; ov.
oviduct; ph. pharynx; pr. profundus nerve; py.
pylorus; st. stomach; symp. sympathetic ganglion
(with suprarenal near it); u.s. urinogenital sinus;
III, V, VII, IX, X, cranial nerves. (From Young,

Quart. J. Micr. Sci. 75.)

i 7 4 ORGANIZATION OF THE HEAD v. 17

the sympathetic, but this is not easy to define in the elasmobranchs
(Fig. no). The vagus, it is true, is well developed, with branches
to the heart and gut, but little is known of autonomic fibres in the
other cranial nerves, or of a special 'sacral' parasympathetic system.
Stimulation of either the vagus or the sympathetic nerves causes
contraction of the stomach. A ciliary ganglion connected with the
oculomotor nerve is present as in other animals, but there is no
sense in which it can be called antagonistic to the sympathetic
system, since the latter does not extend into the head. The post-
branchial plexus is a network of fibres and cells connected with the
vagus but stretching back above the posterior cardinal sinus
(Fig. 104). Receptors in this plexus and in the afferent branchials
(Fig. 109) may be concerned with vascular reflexes (p. 161).

EVOLUTION AND ADAPTIVE RADIATION OF
ELASMOBRANCHS

1 . Characteristics of elasmobranchs

The organization of a shark used to be considered to show the earlier
stages of fish evolution, but we have seen evidence that this is a mis-
take (p. 131). The sharks and skates and rays are highly developed
creatures; in particular, the absence of bone is a secondary feature;
they have been able to give up their defensive armour because of the
development of other means of protection, swift swimming, good
sense-organs and brain, and powerful jaws. We can now examine the
history of these changes and study the varied creatures that can be
classified as elasmobranchs. As usual in examining such histories we
must try to discover evidence about the forces that have operated to
produce the changes of type, and look for signs of any consistent
trends, persisting for long periods of years.

2. Classification

Superclass Gnathostomata
Class Elasmobranchii ( = Chondrichthyes)
Subclass 1. Selachii
*Order 1. Cladoselachii. Devonian-Permian

*CIadoselache; *Goodrichia
*Order 2. Pleuracanthodii. Devonian-Trias

*Pleur acanthus
Order 3. Protoselachii. Devonian-Recent

*Hybodiis; Hetcrodontus
Order 4. Euselachii. Jurassic-Recent
Suborder 1. Pleurotremata. Jurassic-Recent
Division 1. Notidanoidea. Jurassic-Recent
Hexanchus ; Clilamydoselache
Division 2. Galeoidea. Jurassic-Recent

Scyliorhinus; Mustelus; Cetorhinus; Carcharodon
Division 3. Squaloidea. Jurassic-Recent
Squalus; Sqaatina; Pristiophorus ; Alopias
Suborder 2. Hypotremata. Jurassic-Recent
Raja; Rhinobatis; Pristis; Torpedo; Trygon

176 EVOLUTION OF ELASMOBRANCHS vi. 2-3

Superclass Gnathostomata (cont.)

Subclass 2. Bradyodonti. Devonian-Recent
*Order 1. Eubradyodonti. Devonian-Permian

*HeIodus
Order 2. Holocephali. Jurassic-Recent

Chimaera

The elasmobranchs form a very compact group of fishes, nearly
always marine and of predaceous habit, having a great quantity of
urea in the blood, with no bone in the skeleton, no operculum over
the gills, and no air-bladder. The tail is usually heterocercal. The
pectoral fin is anterior to the pelvic and the latter is usually provided
with claspers, fertilization being internal. The body is more or less
completely covered with placoid scales (denticles) and these are
specialized in the mouth to form rows of teeth. The intestine is short
and provided with a spiral valve. The typical cartilage-fishes with
these characters may be placed in the subclass Selachii, to distinguish
them from an early aberrant offshoot the Bradyodonti, represented
today by the peculiar creature Chimaera (p. 184).

3. Palaeozoic elasmobranchs

The selachians are among the most numerous of the various pre-
datory animals in the sea. There have, however, been many side-
branches of the main shark line and we may now survey the history
of the group from its first appearance. The characters we have used
in our definition mark the elasmobranchs off from the earliest-known
gnathostomes, the acanthodians and other placoderm types (Fig. 1 1 1),
which we shall consider later (p. 186). Presumably the elasmobranchs
were derived from some placoderm, but the earliest evidence of the
existence of true sharks is in the form of isolated teeth and scales from
Middle Devonian deposits, and the earliest type about which full
information exists is *Diade?nodus from the Upper Devonian, 'an
early and not distant offshoot from the primitive Chondrichthyan
stock, the main line of which led through *Ctenacanthus and the
hybodonts to the modern elasmobranchs ; *Cladoselache is a specialized
side-line of this main stock and is not an appropriate ancestral type
for the Chondrichthyes' (Harris). The teeth of *Diademodus are
many-cusped and resemble the scales more closely in sculpturing
than in other primitive sharks. The jaw suspension was amphistylic
and the notochord unconstricted. The pectoral fin was continuous
posteriorly with the body wall and there was no well-developed

(i77)

Cenozoic

Cretaceous

100-

Jurassic

Triassic

Perm/an
200

Carbonifcrou.

, t ha

,. .„, Torpedo-

II. HIP

AcMtnedu ^V^vxi L I f)

Silurian

S. *

DieiroleP'i

Ordoi/iaan

400-

Cambrian

FlG. hi. The early evolution of vertebrates.

i 7 8

EVOLUTION OF ELASMOBRANCHS

VI. 3

pectoral girdle. The tail was heterocercal and there are no signs of skele-
tal support for lateral keels. All of these Harris regards as primitive
features; *Diademodus was specialized in having no spines in front
of the dorsal fin and no clasper on the head. Both of these features are
frequent in hybodonts and in *Cladoselache there is a large spine

zd nsi

Fig. 112. Development of the fins of the dogfish, i, Adult showing the nerve-supply
of the fins ; 2, adult with the fins shown expanded and their nerves and muscles shown
as if concentration had not taken place; 3, a 19-mm. embryo, showing the actual

condition.

a. anal fin; ac. anterior collector nerve of first dorsal fin; cr. (black) cartilaginous radial

partially hidden by the radial muscle; n. 1-57, spinal nerves and ganglia; pc. collector

nerve of second dorsal fin; pi. pelvic fin; pt. pectoral fin; rm. radial muscle; id. and 2d.

first and second dorsal fins. (From Goodrich, Vertebrata, A. & C. Black, Ltd.)

in front of the first dorsal fin. These fishes were thus like modern
sharks in their general form, but the fins were remarkable in having
a broad base, not sharply marked off from the body- wall. It has been
suggested by Goodrich and others that this was the earliest condition
of the pectoral fin, perhaps showing its derivation from a continuous
or extended fin-fold (Fig. 113). This theory has the advantage that it
agrees with the embryological development of the fin by concentration
of a series of segments (Fig. 112). It also seems likely that anterior
and posterior fins expanded in the horizontal plane would be neces-
sary for stabilization (p. 136). Moreover, this theory of the origin of
paired fins has the great advantage that it compares them with the
median fins, which are also continuous folds. It has been argued,

vi. 3 PALAEOZOIC ELASMOBRANCHS 179

however, that the cladoselachians are very far from the earliest known
fishes and that in both ostracoderms (p. 125) and placoderms (p. 186)
fins are known that have a narrowly constricted base. We cannot
yet say for certain what has been the course of evolution of the paired
fins, but the fin-fold theory has much plausibility, in spite of the
difficulties raised by palaeontologists.

Fig. 113. Pectoral fins of various fishes.
a, *Cladoselache\ b, *Pleur acanthus; c, Ncoccratodus; d, Gadits. (From Norman.)

The cladoselachians represent the ancestral Devonian sharks, from
which all later forms have been derived. Animals of similar type
were fairly common in late Devonian and Carboniferous seas. The
ctenacanths, such as *Goodrichia, reached a length of 8 ft. Later
radiation of the selachians took place along three different lines,
represented by the three remaining orders shown in the classification.
The pleuracanthodians (*Pleuracanthus) were a specialized group of
freshwater carnivores. The tail was straight (diphycercal) and the
paired fins had become modified accordingly (see p. 137). The axis
was completelv freed from the body wall to give a paddle-like fin,
with pre- and post-axial rays, a type known as archipterygial (Fig.
113), because it was once supposed to be ancestral to all others. A
large spine on the head gives the group its name. Claspers were pre-
sent. These animals were common in the Carboniferous and Lower

180 EVOLUTION OF ELASMOBRANCHS vi. 3-

Permian, but in subsequent times they disappeared without leaving
descendants.

4. Mesozoic sharks

After flourishing in Palaeozoic seas the shark line seems to have
become nearly extinct during the Permian and Trias. During this
period there was probably little fish life in the sea and the stock
seems only to have survived by adopting a varied diet, including
invertebrate food. The protoselachian or heterodont sharks of this
period had two types of tooth, pointed ones in front and flattened
ones, for crushing molluscs, behind. Heterodontus, the Port Jackson
shark of the Pacific, is a surviving form having a dentition of this
type.

There is total cleavage of the yolk of the egg. The meroblastic form
typical of modern elasmobranchs and teleosts was therefore a rela-
tively late development and other survivors of the mesozoic period
besides Heterodontus also show holoblastic cleavage (pp. 184-236). In
later Triassic times sharks again became more abundant, and this
agrees with the presence of numerous bony fish types, on which they
presumably fed. Some of the Triassic sharks still possessed a hetero-
dont dentition (*Hybodus), though otherwise much like the modern
forms.

In Jurassic times or earlier, however, the sharks divided into the
main lines that exist today. In the suborder Pleurotremata or true
sharks the teeth all became sharp and the animals swift swimmers. In
the suborder Hypotremata, on the other hand, the teeth remained
flattened and sometimes became highly specialized for a mollusc-
eating diet (Fig. 1 14), producing the flattened bottom-living creatures,
the skates and rays. The stages of this transition can be followed, and
some of the intermediate types still exist. Thus in Rhifiobatis, the
banjo-ray (Fig. in), the pectoral fins are enlarged but still distinct
from the body. Almost identical creatures have been found in Jurassic
rocks. It is probable that several separate lines showed this flattening
of the body.

5. Modern sharks

The Pleurotremata may be divided into three divisions all dating
from the Jurassic. The Notidanoidea show many primitive features,
such as an amphistylic jaw, the presence of six or seven gill-slits, and
an unconstricted notochord. Hexanckus and Heptranchias, are long-
bodied, slow-moving sharks from warm waters. They are viviparous

vi. 5

SHARKS

181

but without placentae. Chlamydoselache, the frilled shark, lives in
deep water and feeds on cephalopods. The division Galeoidea is much
larger and includes the sharks with two dorsal fins, not supported by
spines. Here belong the dogfishes Scyliorhinus and Miistelus, both
mainly bottom-living animals feeding on a mixed diet, including

Fig. 114. Teeth of various elasmobranch fishes.

1, Man-eater (Carcharodon); 2, tiger shark (GalaeocerJo); 3, comb-toothed shark (Hexanchus);

4, sand-shark (Odontaspis); 5, blue shark (Carcharinus); 6, nurse shark (Ginglymostoma);

7, guitar rish (Rhina), 8, eagle-ray {Myliobatis), (After Norman.)

crustaceans and molluscs. In Cetorhimis, the basking shark, the pre-
daceous habit of the group has been abandoned in favour of straining
small food directly from the plankton by means of special combs on
the gills (gill rakers), an arrangement recalling that of the whalebone
whales. The great effectiveness of this method of feeding may be seen
in the length of 35 ft or more attained by some of these sharks. Bask-
ing sharks produce very numerous small eggs, which develop within
an 'uterus', but without placentae. Rhineodon, the whale shark, is also

1 82 EVOLUTION OF ELASMOBRANCHS vi. 5-6

a plankton feeder and becomes very large. It is not closely related to
the basking sharks. It moves up and down vertically, the mouth open,
sucking in plankton. In this group there are also many of the fiercest
man-eating sharks, such as Carcharodon, often 30 ft long, found in
many seas. Some fossil forms of this genus are estimated to have
reached a much greater length, possibly of 90 ft.

The division Squaloidea includes those sharks in which there is
a spine in front of each dorsal fin. They are not, however, otherwise
different in habits from the other sharks. The spiny dogfish (Squalus)
is a well-known type and here belong also the saw-sharks (Pristio-
phorus) and a group of bottom-living forms, the angel-fishes or monks
[Squatina), which acquire a superficial similarity to the skates and
rays. Alopias, the thresher, is said to differ from most sharks in that
instead of seizing the prey as it is presented, it hunts systematically,
several sharks working together and using their whip-like tails to
drive smaller fishes such as mackerel into shoals, where they are then
seized.

6. Skates and rays

The Hypotremata, skates and rays, have become specialized for
life on the bottom of the ocean in shallow waters, feeding mainly on
invertebrates, and usually having blunt teeth (Fig. 114). Locomotion
is no longer by transverse movements of the body but by waves that
pass backwards along the fins. In the earlier stages, such as Rhino-
bath, the banjo-ray, which has existed from the Jurassic period to the
present, the edges of the fins are still free and the tail is well developed.
In Pristis, another saw-fish type, outwardly similar to Pristiophorus
and known since the Cretaceous, the head is drawn out into a long
rostrum armed with denticles. Its use is uncertain but the head strikes
from side to side among shoals of fishes. There are species in India,
China, and the Gulf of Mexico that live in fresh water. In Raja, first
found in the Cretaceous, the pectoral fins are attached to the sides of
the body and the median fins are very small, whereas in the more
recent Trygon and other sting-rays the tail is reduced to a defensive
lash, the dorsal fin persisting as a poison spine. In the eagle-rays
(Myliobatis) the teeth are flattened to form a mill able to grind mollusc
shells (Fig. 114). The sea-devils (Mobula) have expansions of the fins
at the front of the head, which they use to chase fishes to the mouth,
hunting in packs. In Torpedo, the electric ray, the fins extend so far
forward that the front of the animal presents a rounded outline. The
animal is protected by a powerful electric organ, formed by modified

(i8 3 )

Torpedo

Raja

FIG. 115. Various elasmobranch. fishes.

Chimaera ^ T

184 EVOLUTION OF ELASMOBRANCHS vi. 6-

latcral plate muscle, innervated by cranial nerves. Several species of
Raja have weak electric organs perhaps used for guidauce (p. 253).

Life on the bottom has produced many further modifications in the
skates and rays. In those that live in shallow and hence well-illuminated
waters the colour of the upper surface is often elaborate, the under
side being white. In certain species of Raja, for example, there is a
pattern of black and white marks, which probably serves to break up
the outline of the fish.

The eyes of the skates and rays have moved on to the upper surface
of the head and are protected by well-developed lids. In most forms
the pupil is able to vary widely in diameter and often has an operculum
by which the aperture can be reduced to two small slits.

There is a special modification of the respiratory system so that
water is drawn in not through the mouth but by the spiracle, which is
provided with a special valve that shuts at expiration, as the water is
forced out over the gills. The Hypotremata have therefore developed
many special features for their bottom-living habits and have diverged
among themselves into many varied lines. They have been very
successful and are among the commonest fishes in the sea.

7. Chimaera and the bradyodonts

Finally we must consider an aberrant group, the bradyodonts, which
diverged from the main stock at least as early as the Carboniferous
and preserves for us today some features of elasmobranch life at that
time as the strange Chimaera, the rat-fish of deep seas (Fig. 115).
Instead of the usual large, toothed mouth these Holocephali have a
small aperture surrounded by lips, giving the head a parrot-like
appearance. The teeth are large plates firmly attached to jaws, and
the upper jaw is remarkable in being fused to the skull ('holostylic'),
the hyoid arch being free. There is no stomach or spiral intestine.
These peculiarities are probably associated with a capacity to eat
small pieces of animal food. The Holocephali differ further from the
Selachii in the presence of an opercular flap attached to the hyoid
arch. There are also extra claspers in front of the usual pelvic ones
and an organ on the head of the male known as the cephalic clasper,
whose function is obscure. The notochord is unconstricted and the
vertebrae reduced to separate nodules. The cleavage is holoblastic,
as in other fishes with features of mesozoic type (p. 180).

Many of the internal features resemble those of selachians, for
instance the conus arteriosus, and urinogenitals in which there are
separate urinary and spermatic ducts. The brain has a peculiar shape

vi. 8 TENDENCIES IN EVOLUTION 185

on account of the large size of the eyes, which almost meet above the
brain, so that the diencephalon is long and thin.

These strange creatures appear in the Jurassic, apparently de-
scended from the somewhat similar bradyodonts (such as *Helodus),
which were common in the Carboniferous and Permian. They pre-
serve some primitive features (vertebrae, jaw support, open lateral
line canals, cleavage) but have developed many specializations in the
teeth, operculum, fins, and brain, probably in connexion with life on
the bottom of deep seas.

8. Tendencies in elasmobranch evolution

The elasmobranchs have been in existence ever since the Devonian,
and for much of this long period of nearly 400 million years we can fol-
low their changes with some accuracy. This type of fish was first
formed by loss of the heavy bony armour of the earliest gnatho-
stomes, associated with the adoption of a rapidly moving and car-
nivorous habit. The resulting shark-like form has remained with
relatively little change through the whole history of the group; clado-
selachians from the Devonian are remarkably like modern sharks, and
it would be difficult to assert that the latter show clear signs of being
in any way of a 'higher' type. Both are in fact suited to the same mode
of life.

If our interpretation of the evidence is right, however, the modern
shark type has been evolved from the Devonian type through a hetero-
dont stage. During the late Permian and Trias there was little fish
food for the sharks and they appear to have taken to living on inverte-
brates. Eating this diet was presumably easier for animals possessing
the two types of teeth described on p. 180, and the animals also
became rather flattened with their life on the bottom. On the
reappearance of numerous fishes in the sea, in the Jurassic, some of
these heterodonts resumed the shark-like habit, lost the crushing
teeth, and developed into the varied fish-eating types alive today.
Others of the heterodonts, however, became still more specialized for
bottom life, as the modern skates and rays.

It is difficult to see any persistent tendency in all this, except to eat
other animals of some sort. When fishes are available sharks will eat
them, and the bodily organization for doing so seems to have been
evolved at least twice. Similarly other members of the same stock ate
molluscs and Crustacea and became modified for this. The tendency
is for survival or continuance of the animals and this leads them
to adopt whatever habits are possible given their surroundings. In

i86 EVOLUTION OF ELASMOBRANCHS vi. 8-

meeting the circumstances certain types will be suitable at one time,
others at another. We know that genetic variations will produce fluctua-
tions of type — at a time when circumstances force the animals to strive
in one direction those with a particular bodily type, say, broad, 'hetero-
dont' teeth will be selected. When fish food again becomes available
those animals born with quicker habits and sharper teeth will be able
to eat the fish and the shark type returns.

The method of ensuring stability in the pitching plane adopted by
elasmobranchs (p. 136) necessitates a certain flattening of the front
end of the animal. It is not therefore surprising that this tendency is
often exaggerated and has several times produced flattened bottom-
living creatures, such as the skates and rays. The Actinopterygii
show the opposite tendency, to lateral flattening (p. 248). We might
imagine that most of the modern skates and rays had become so
modified in structure that only life on the bottom is possible for them
and that there could be no return to a free-swimming, fish-eating
habit, but it would not be true to say that this is certain or that the
past history of the group shows undoubted evidence of such irrever-
sible specialization.

The only general conclusion from our study of elasmobranchs since
the Devonian, then, is that they have tended to keep alive by eating
fish or invertebrates, that some have changed little during this time
but that, judging especially from the modern forms, the group tends
to produce varied types at any one time, each able to find its food in a
special manner. It is not clear that the group has advanced, in any
sense, since the Devonian. The type has always been a successful one,
able to produce specialized carnivores. We do not know enough to be
sure whether the number of creatures with this organization has
changed greatly, but it seems that, except for a reduction in numbers
in the Triassic, they have always been moderately abundant and are
perhaps at present on the increase.

9. The earliest Gnathostomes, Placoderms

*Class Placodermi (= Aphetohyoidea)

*Order 1. Acanthodii. Silurian-Permian (*Climatius)
*Order 2. Arthrodira. Silurian-Devonian (*Coccosteus)
*Order 3. Macropetalichthyida. Devonian (*Lunaspis)
*Order 4. Antiarchi (= Pterichthyomorphi). Devonian (*Bothri-

olepis)
*Order 5. Stegoselachii. Devonian-Carboniferous (*Gemundina)
*Order 6. Palaeospondyli. Devonian {* Palaeospondylus)

vi. 9 PLACODERMS 187

It has already been mentioned that the earliest gnathostome verte-
brates found in the rocks do not have the shark-like form, and present
so many peculiarities that they are placed in a distinct class. In the
past the fossils included here have been referred to various groups,
usually either to the agnatha or the elasmobranchs, and there is still
some doubt as to their position. In many respects they are highly
specialized, but they all have one feature that may be presumed to
have existed in the ancestral gnathostome, namely, that the hyoid arch
played no part in the support of the jaws and the spiracle was there-
fore a typical gill-slit. For this reason they are often given the name
Aphetohyoidea, but we shall prefer to call them Placodermi, to em-
phasize that they all have a heavy armour of bone-like material. The
class contains several orders, not obviously very closely related to
each other; all are fossil forms, none of which is known to have sur-
vived the Permian.

The best-known, earliest, and perhaps most interesting group is
the acanthodians, found in freshwater deposits extending from the
Upper Silurian to the Permian but chiefly in the Devonian. These
were small fishes with a fusiform body (Fig. 115), with heterocercal
tail and two, or later one, dorsal fins. The lateral fins consisted of a
series of pairs, often as many as seven in all, down the sides of the
body. The effect of these in stabilizing the fish would presumably be
different from that of a continuous fold, and the problem of the form
and function of the earliest paired fins remains obscure. The fins were
all supported by the large spines from which the group derives its
name.

The whole surface of the body was covered with a layer of small
rhomboidal scales, composed of layers of material ressembling bone,
covered with a shiny material similar to the ganoin of early Actino-
pterygii. On the head these scales were enlarged to make a definite
pattern of dermal bones, numerous at first but fewer in the later forms.
The pattern of the bones has no close similarity to that of later fishes.
The reduced bones of the later acanthodians are related to the lateral
line canals, which have an arrangement similar to that in other fishes,
but run between and not through the scales and bones of the head.
The teeth are formed as a series of modified scales. The skull is partly
ossified — important evidence that the boneless condition of elasmo-
branchs was not typical of all early gnathostomes.

The jaws of acanthodians were attached by their own processes to
the skull (autodiastyly) and are remarkable in that four separate
ossifications take place in them (two in the upper and two in the lower

1 88 EVOLUTION OF ELASMOBRANCHS vi. 9

jaw), making a series of elements similar to that found in the typical
branchial arches. The hyoid was an unmodified branchial arch. At
first the mandibular, hyoid, and each of the branchial arches were pro-
vided with small flap-like opercula, but in later forms the mandibular
operculum became especially developed and covered all the gills.

These animals might well represent the ancestors of many if not all
other groups of gnathostomes. They have not the peculiar features
that we characterize as shark-like, and though they may well have
been carnivorous they are not very highly specialized for that mode of
life. Whether or not the known acanthodians represent the actual
ancestors of the other gnasthostome groups, it is clear that knowledge
of their anatomy forces us to discard two conclusions which have
often been accepted in the past, namely, that lack of bone and an
amphistylic jaw support are primitive gnathostome features. Here
already in the Silurian we find animals that possessed both endo-
chondral bone and scales composed of bony substance. Moreover,
some of them have no trace of denticles and we must therefore regard
with suspicion any theory that considers the placoid scale as the
original type of all scales. It is at least as likely that scales composed of
simple layers of bone in the dermis were the ancestral type and that
placoid forms with a pulp cavity were a later specialization.

Several other types of placoderm fish are known, mostly from the
Devonian strata. The Arthrodira, Macropetalichthyida, and Anti-
archi (Fig. in) were mostly heavily armoured fishes with dermal
bones on the head and often a large shield over the body. There was
usually a heterocercal tail and a covering of scales. The earlier fishes
were mostly from fresh water, the later from the sea. Many were
rather flattened, probably bottom-living and invertebrate-eating
forms. The bony plates on the head were often arranged in charac-
teristic patterns, none of which, however, shows close similarity to
the pattern of bones on the head of bony fishes or tetrapods. Lateral
line canals of typical arrangement were present and the 'bones' follow
these to some extent.

*Gemundina was a flattened animal, superficially similar to a skate,
from marine Lower Devonian deposits. The skin was covered with
denticles, but under these were large plates, apparently of bone. This
fish is placed in a special order Stegoselachii and its affinities are
unknown, but it shows again that the tendency to develop a flattened
form has been present from the earliest appearance of fishes. *Palaeo-
spondylus from the Devonian is another isolated form, in the past often
classed with the cyclostomes. Moy-Thomas showed, however, that

vi. 9 PLACODERMS 189

jaws were present and that probably the hyomandibula was not sus-
pensory. He therefore classed the fish with the placoderms, in spite
of the absence of any dermal skeleton. So far as can be discovered,
all these placoderm fishes except the acanthodians were specialized
types and have not left any later descendants. Indeed it may well be
that they have been preserved only because of the great extent of their
armour; less heavily protected relatives may have existed but have
not survived as fossils. The remains that are known are sufficient to
establish the fact that there were, in the Devonian period, numerous
types of fish possessing a bony skeleton.

VII

THE MASTERY OF THE WATER. BONY FISHES

1 . Introduction : the success of the bony fishes

The acanthodians and some other of the late Silurian and Devonian
gnathostome fishes possessed bony skeletons; from these, or some
placoderm animals like them, may have been derived not only the
elasmobranchs but also the bony fishes and the lung-fishes, which
gave rise to the land animals. These presumed descendants of the
placoderms can be divided into three groups : first the elasmobranchs,
secondly, the crossopterygians, the lobed-fin or lung-fishes, including
the Devonian forms that led to the amphibia, and thirdly, the actino-
pterygian or rayed-fin fishes, culminating in the modern bony fishes.
In Devonian times the Crossopterygii and Actinopterygii were very
alike and both, like the placoderms, contained bone. The term bony
fishes or Osteichthyes is often applied to these two groups together,
since they have some features in common and distinct from the
elasmobranchs.

The great group of Actinopterygii, which, for all the importance of
the elasmobranchs, must be reckoned as the dominant fish type at the
present time, includes most of our familiar fishes, perch, pike, trout,
herring, and many other types of 'modern' fish. In addition there are
placed here some surviving relics of the stages that have been passed
before reaching this condition, such as the bichir, sturgeons, bow-fin,
as well as related fossil forms.

Many groups of animals have been successful in the water; Crus-
tacea, for instance, are very numerous and so are cephalopod molluscs
and echinoderms, but the success of the bony fishes surpasses that of
all others. From a roach or perch in a stream, to a huge tunny or a vast
shoal of herrings in the sea, they all have the marks of mastery of the
water. They can stay almost still, as if suspended, dart suddenly at
their prey or away from danger. They can avoid their enemies by
quick and subtle changes of colour. Elaborate eyes, ears, and chemical
receptors give news of the surrounding world and complex be-
haviour has been evolved to meet many emergencies. Reproductive
mechanisms may be very complex, involving elaborate nest-building
and care of the young; social behaviour is shown in swarming move-
ments, which may be accompanied by interchange of sounds (p. 217).

vii. 1-2 THE TROUT 191

Bony fishes abound not only in the sea but also in fresh water,
which has never been effectively colonized by cephalopods or elasmo-
branchs. They can exist under all sorts of unfavourable or foul-
water conditions and a considerable number of them breathe air and
live for a time on land. Perhaps the majority are carnivorous, but
others feed on every type of food, from plankton to seaweeds.

To whatever feature of fish life we turn we find that the bony fishes
excel in it in several different ways in different species. It is small
wonder that with all these advantages they are excessively numerous.
There are some 3,000 species of living elasmobranchs, but more than
20,000 species of bony fish have been described.

The number of individuals of some of the species must be really
astronomical. For instance, at least 3,000 million herrings are caught
in the Atlantic Ocean each year, so that the whole population there
can hardly be less than a million million. Again, it is estimated that a
thousand million blue-fish collect every summer off the Atlantic coast
of the United States and, being very voracious carnivores, they con-
sume at least a thousand million million of other fishes during the
season of four months. This gives some idea of the tremendous
productivity of the sea, and of the way the bony fishes have made
use of it. Needless to say, man has also made considerable use of the
bony fishes, which indeed provide, with the elasmobranchs, a not
inconsiderable portion of the total of human food.

2. The trout

Salmo trutta, the brown trout, may be taken as an example of a bony
fish; we shall also refer at intervals to conditions in other common
freshwater fish such as the dace, Leuciscus, and perch (Perca fluvi-
atilis). There is considerable confusion about the various types of
trout and their close relatives the salmon. The brown trout is abundant
in rivers and streams throughout Europe and is commonly about
20 cm long at maturity, though it may grow larger. It is grey above
and yellowish below, with a number of dark spots scattered down
the sides of the body (Fig. 116).

The body form is typical of that of teleostean fishes in being short,
narrow in the lateral plane but deep dorso-ventrally, in fact more ob-
viously streamlined than the shape of elasmobranchs. The movements
of a trout do not at first sight obviously involve the bending of the body
into an S; nevertheless, the method of swimming is essentially by the
propagation of waves along the body by the serial contraction of the
longitudinally directed fibres of the myotomes (p. 133).

192

BONY FISHES

VII. 2-

The tail differs from that of elasmobranchs in being outwardly
symmetrical, though internally there are still traces of the upturned
tip of the vertebral column (Fig. 118). Besides the typical caudal
'fish-tail', supported by bony rays, there are two dorsal fins and a
ventral fin, but the hinder dorsal fin differs from the others in having
no rays to support it and is called an adipose fin, because of its flabby
structure. The paired fins are rather small and it is from their struc-
ture that the whole group derives the name Actinopterygii or rayed-fin
fishes. There is no lobe projecting from the body and containing

Fig. i i 6. Male and female brown trout (Salmo trutta) spawning. The male is quivering — a

short sequence of rapid shudders of whole body which excites the female.

(After J. W. Jones, The Salmon.)

basal fin supports, as there is in the fin of lung-fishes. All the basal
apparatus of the fin is contained within the body wall and only the fin
rays project outwards, as a fan. The pelvic fin of bony fishes often
lies relatively far forward; in the trout, however, it is unusually far
back, just in front of the anus; in other types it may be level with the
pectoral fin, or even anterior to it (Fig. 118). The significance of the
shape of the body and fins in swimming will be discussed later (p. 244).
The skin consists of a thin epidermis and thicker dermis, the former
has stratified squamous layers but contains no keratin (Burgess, 1958).
It contains mucous glands. The mucus of some eels and other fishes
has remarkable powers of precipitating mud from turbid water. The
mesodermal dermis provides an elaborate web of connective tissue
fibres. It also contains smooth muscle, nerves, chromatophores, and
scales. The latter are thin overlapping bony plates, covered by skin,
that is to say, they do not 'cut the gum' as do placoid denticles. The
exposed part of each scale bears the pigment cells, which control the
colour of the animal, in a manner presently to be described. The bone
of the scales is absorbed at intervals by scleroclasts, making a series
of rings, which, like the growth-rings on a tree, are due to the fact
that growth is not constant but occurs fast in the spring and summer

VII. 3

FISH SCALES

193

and hardly at all in the winter. The age of the fish can therefore be
determined from these rings (Fig. 117), or from the similar markings
on the ear stones (p. 216). While an adult salmon is in fresh water no
growth occurs, leaving a spawning mark on the scale.

The head of the trout shows some of the most specialized and typical
teleostean features (Fig. 119). There are two nostrils on each side, but
no external sign of ears. The mouth is very large and its edges are
supported by movable bones, to be described below. The maxillary
and mandibular valves are folds
of the buccal mucosa, serving to
prevent the exit of water during
respiration. The tongue, as in
Selachians, has no muscles, but
may carry teeth and taste-buds.
Behind the edge of the jaw is the
operculum, a flap covering the
gills and also supported by bony
plates. In connexion with these
special developments of jaws and
gills the skull has become much
modified and has developed com-
plex and characteristic features
(Fig. 118).

Fig. 117. Spawning mark (sp. ?nk.), the
result of erosion or absorption of the scale
margin due to a calcium deficiency fasting
period. (After J. W. Jones, The Salmon.)

1st river winter. 2. 2nd river winter.
3. 1 st sea winter.

3. The skull of bony fishes

The main basis for the skull
is a chondrocranium and set of

branchial arches, exactly comparable to those of the elasmobranchs.
In the early stages of development there is a set of cartilaginous boxes
around the nasal and auditory capsules, brain and eyes, and a series
of cartilaginous rods in the gill arches. Bones are then added in two
ways: either (i) as cartilage bones (endochondral bones) by the re-
placement of some parts of the original chondrocranium, or (2) as
membrane or dermal bones, laid down as more superficial coverings
and considered to be derived from a layer of scales in the skin. This
outer position of the bones can be clearly seen in many cases by the
readiness with which the membrane bones can be pulled away from
the rest of the skull.

The skull bones are arranged in a regular pattern, whose broad
outlines can be seen in all fishes and in their tetrapod descendants.
However, there are many confusing variations and the naming of

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vii. 3 SKULL OF TELEOSTS 195

bones has given much controversy. No generally acceptable theory
has yet appeared, perhaps because we know little of the factors that
cause separate bony elements to develop. There is some evidence of
relations between bones and teeth and bones and lateral line organs
and the pattern of the latter may play a large part in determining the
plan of the skull (p. 325). Provisionally we may recognize four classes
of dermal bones (1) canal bones, (2) tooth bones, (3) 'ordinary' bones,
whose determination is unknown, (4) extra bones, filling special areas
(Wormian bones).

The arrangement of the numerous bones is made less difficult to
understand and remember if they are considered in the following
order. First the endochondral ossifications in the original neuro-
cranium, then the dermal bones that cover this above and below; next
the endochondral bones formed within the original cartilaginous jaws,
then the dermal bones that cover the edges of the jaws, and finally the
ossifications in the branchial arches and pectoral girdle, which latter
is in bony fishes attached to the skull.

The endochondral ossifications may be considered by beginning at
the hind end of the skull: here the floor ossifies as the basioccipital,
the sides as the exoccipitals, and the roof, over the spinal cord, as the
supra-occipital bone; these posterior bones are not well marked off
from each other in the adult skull. In the auditory capsule are five
separate otic bones, of these the epiotic and pterotic can be seen
externally (Fig. 118).

The floor in front of the basioccipital is occupied by a basisphenoid
bone and the walls above this by alisphenoids. The eyes nearly meet in
the midline and the orbits are here separated only by a thin orbito-
sphenoid. The only more anterior part of the chondrocranium to
ossify is the region between the nasal capsule and the orbit, forming
the ectethmoid.

The dermal bones that cover this partly ossified neurocranium may
be identified as on top and in front a pair of frontals and a median
supraethmoid, behind which are large paired parietals and small
paired post-parietals. These names have been inferred from study of
crossopterygians and early amphibians (p. 325), which showed that
the homologies earlier accepted were wrong. Fig. 118 carries the old
nomenclature in which the large paired bones were called frontals.
Around the eyes is a ring of circum-orbitals, and on the floor of the
skull two median bones, the parasphenoid and vomer.

The jaw bones are numerous, including both endochondral and
dermal elements, and the relation of the method of support to that

196 BONY FISHES vn. 3-

found in other animals is not clear. In the embryo palato-pterygo-
quadrate bars and Meckel's cartilages are seen. The upper jaw bears
inward projections, which extend towards the chondro-cranium and
probably represent the traces of an autostylic means of support (see
p. 187). But the effective support in the adult is achieved by the ossi-
fied hyomandibular cartilage. The palato-pterygo-quadrate bar ossifies
in several parts and palatine, pterygoid, mesopterygoid, metaptery-
goid, and quadrate bones appear, some of them partly formed in mem-
brane. The only part of Meckel's cartilage to ossify is the articular
bone, at the hind end. The actual edges of the jaws are supported by
membrane bones, the premaxilla, maxilla, and jugal, covering the
upper jaw. The dentary covers most of the lower jaw, except for a
small bone, the angular, that lies on the inner side at the posterior end.

The hyomandibular bone runs from an articulation with the otic
capsule to the upper end of the quadrate. The symplectic is a small
separate ossification at the lower end of the hyomandibula. The rest
of the hyoid arch is present as epi-, cerato-, and hypohyals, which
support a large toothed tongue. Bony fishes only rarely possess an
open spiracle and immediately behind the hyoid are attached the
bones supporting the operculum that covers the gills. The branchial
arches are formed of several pieces, as in elasmobranchs, each being
ossified separately.

The effect of this complicated set of bones is to provide an efficient
apparatus for the protection of the brain and sense-organs, support
of the jaws and teeth and of the respiratory apparatus. Teeth are found
on the vomers, palatines, premaxillae, maxillae, dentary, and on the
tongue. Covering the typical dentine (orthodentine) is a layer of
harder vitrodentine, poor in organic matter and perhaps derived
partly from ectodermal ameloblasts. The teeth are usually spikes
pointing in a backwards direction, used to prevent the escape of the
food and not usually for biting or crushing. They may, however, form
plates or be firmly attached to the bones. Folds of the mucous mem-
brane, supported by cartilage and carrying gill-rakers, are found in
species that feed on small prey.

4. Respiration

Limitations are imposed on the respiration of fishes by the facts
that water is 800 times more dense than air and the dissolved oxygen
is 30 times more dilute. The cost of respiration is therefore high. There
is a 70 per cent, increase in metabolism when a trout increases its
ventilation volume four times in water poor in oxygen.

vir. 4

RESPIRATION

197

Respiration is produced by a current passing in a single direction,
as in elasmobranchs, namely, in at the mouth and out over the gill
lamellae, but the mechanism by which the current is produced is some-
what different. The pumping action is produced by a buccal pressure
pump and opercular suction pumps, resulting from sideways move-

A B

Fig. 119. Arrangement of organs of head and gills in A, a shark, and,

B, a teleostean fish.

gb. gill bar; GC. outer opening of gill cleft; GF. gill filament; gr. gill-rakers; cv. gill vessels;

J, ]'. upper and lower jaw; M. mouth; N, n'. openings of nasal chamber; op. operculum;

sp. spiracle; ST. septum between gill filaments. (From Dean, Fishes, Living & Fossil,

The Macmillan Co.)

ments of the operculum, enlarging the branchial cavity. The branchio-
stegal folds, below the operculum, prevent inflow of water from
behind. When the operculum moves inward dorsal and ventral flaps
in the throat prevent the exit of water forwards.

The gill lamellae differ from those of elasmobranchs in the great
reduction of the septum between the respiratory surfaces (Fig. 119).
This has the effect of leaving the lamellae as free flaps, increasing the
surface available for respiration.

The area of the gills varies greatly, being relatively larger in more
active species. The rate of respiration is controlled by a medullary
centre but the most active rate of respiratory exchange is only some
four times the standard rate (as against twenty times in man). The

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vii. 4-5 BACKBONE OF FISHES 199

area of the respiratory surface is thus an important limiting factor in
the movement and growth of fishes. During activity of a fish lactic
acid accumulates in the blood and the pH falls. The fish is thus able
to display a considerable burst of activity and then to repay the
oxygen debt over a long subsequent period.

5. Vertebral column and fins of bony fishes

The vertebral column of bony fishes performs the same function as
in other fishes, namely, to prevent shortening of the body when the
longitudinal muscles contract. It has, however, become very compli-
cated and with the ribs and neural and haemal arches forms an
elaborate system serving to maintain the body form under the stresses
of fast swimming. Like other parts of the skeleton it is extensively
ossified, and the necessary lateral flexion is obtained by division of
the column into a series of sections joined together. Typically there
is one such section (vertebra) corresponding to each segment, but in
the tail region of Amia there are twice as many vertebrae as segments.

Each vertebra consists of a centrum, neural arch and neural spine,
and in the tail region, in addition, haemal arch and haemal spine.
These parts are formed partly by ossification of cartilaginous masses,
the basidorsal and basiventral, interdorsal and interventral, such as
we saw in elasmobranchs, and partly by extra ossification in the sclero-
genous tissue around the notochord and nerve-cord and between the
muscles. The vertebrae are inter-segmental, the middle of each lying
opposite the myocomma that separates two muscle segments.

The centra are concave both in front and behind (amphicoelous),
and in the hollows between them are pads made of the remains of the
notochord, an arrangement that allows the column to resist longi-
tudinal compression and yet remain flexible; similar flat or concave
articulations of the centra are found in other aquatic vertebrates from
the elasmobranchs to the whales. Extra processes on the front and
back of the vertebrae ensure the articulation and are comparable to the
zygapophyses found in tetrapods. The ribs, which are so prominent
in the backbone of many fishes, are of two sorts; pleural ribs between
the muscles and the lining of the abdominal cavity, and more dorsal
intramuscular ribs. Both sorts are attached to the centrum. The bony
rods attached above the neural and below the haemal arches are often
called neural and haemal spines, though it is doubtful whether they
correspond to the neural spines of land vertebrates. They form the
supporting rods or radials of the median fins and are usually divided
into two or three separate bones in each segment. In addition to these

200

BONY FISHES

vii. 5-

radials the fins are also supported by a more superficial set of bony-
rods, the dermal fin rays (dermotrichia or lepidotrichia), which may
be considered as modified scales and accordingly lie superficial to the
radials. These dermal fin rays are usually forked at their tips. They
make an extra support for the fin margin and to them are attached the
muscles that serve to throw the fin into folds.

In the tail region the internal skeleton is not quite symmetrical and
shows signs of origin from an animal with a heterocercal tail. The

<ev.msx.

3<j-mand.

Fig. 121. Muscles of a teleostean fish, mainly based on Mullus.
ad-mand. adductor mandibulae; ep. epaxonic muscles; h. horizontal myoseptum; hy. hypo-
branchial muscles; hyp. hypaxonic muscles; lev. max. levator maxillae; my. myocomma;
op. operculum. (From Ihle.)

notochord turns up sharply at the tip, so that the neural spines are
very much shorter than the haemal spines, known here as hippural
bones. The final portion of the notochord is often surrounded by a
single ossification, the urostyle, and the whole makes a rigid support
for the dermotrichia of the tail. Such a tail with internal asymmetry
but external symmetry is said to be homocercal.

The myotomes are arranged in a complicated pattern having the
effect that contraction of each affects a considerable section of the
body (Fig. 121); in fast swimmers such as the tunny each myotome
may overlap as many as nineteen vertebrae. Between the lateral and
ventral muscle masses there is in many fishes a layer of red muscle
and this is especially well developed in the tunnies and bonitos.

The paired fins are similarly supported by ossified radials, covered
by dermal fin rays. At the base the radials are connected with 'girdles'
lying in the body wall. The pectoral girdle (Fig. 118) consists of a
cartilaginous endo-skeletal portion in which ossify the scapula, cora-
coid, and sometimes mesocoracoid, while dermal bones, large cleith-
rum, and one or more small clavicles, become attached superficially.

vii. 8 ALIMENTARY CANAL 201

Above these a further series of dermal bones, the supra-clavicle and
post-temporal, attach the pectoral girdle to the otic region of the skull.
The pelvic girdle is very simple, consisting only of a single bone,
the basipterygium.

6. Alimentary canal

The food of the trout consists mainly of small invertebrates such as
Gammarus, Cyclops, and other crustaceans, and aquatic insects and
their larvae, together with the fry of other fishes and perhaps some-
times larger pieces of 'meat'. The food is mostly swallowed whole,
being helped down the pharynx by the mucous secretions, but these,
as in elasmobranchs, contain no enzymes. The entrance to the stomach
is guarded by a powerful oesophageal sphincter, no doubt serving to
prevent the entry of the water of the respiratory stream. The stomach
is divided into cardiac and pyloric portions, though the distinction is
less clear than in elasmobranchs. The duodenum is beset by a number
of wide-mouthed pyloric caeca, serving to increase the intestinal
surface (Fig. 120). The intestine and caeca are lined throughout by a
simple columnar epithelium and there are no specialized multicellular
glands such as the Brunners glands or crypts of Lieberkiihn of mam-
mals. The exocrine pancreas consists of numerous diffuse glands in
the mesentery. The endocrine portion, however, forms a compact
mass of tissue. This is very rich in insulin and after its removal a fish
shows hyperglycemia and glycosuria. The intestine is relatively longer
than in elasmobranchs and often coiled; its internal surface may be
increased by folds, but there is no true spiral valve, though this was
present in the ancestors of the Teleostei (p. 233). There is no gland
attached to the rectum.

7. Air-bladder

Dorsal to the gut is a very large sac with shiny, whitish walls, the
air-bladder, filled with oxygen. A narrow pneumatic duct connects
this with the pharynx in the more primitive forms. The origin and
functions of the air-bladder will be discussed below (p. 261); it serves
as a hydrostatic organ, enabling the animal to remain suspended in
the water at any depth.

8. Circulatory system

The general plan of the circulation is similar to that of an elasmo-
branch (Fig. 122), that is to say, there is a single circuit and all
the blood passes through at least two sets of capillaries. The heart

202 BONY FISHES vu. 8-

contains a series of three chambers, sinus, auricle, and ventricle, but the
muscular conus arteriosus is absent, there being only a thin-walled
bulbus arteriosus at the base of the ventral aorta. The walls of the
bulbus are elastic but not muscular, and study of its action by means
of X-rays shows that it is dilated by the ventricular beat and then
contracts, thus maintaining the pressure against the capillaries of the
gills. The ventral aorta is short, but the arrangement of the afferent
and efferent branchial vessels is essentially as in elasmobranchs.

The blood-pressure in the ventral aorta is less than 40 mm Hg in
most fishes at rest, and in the dorsal aorta about half this. The venous
pressures are around zero, the pericardium being fibrous but not
rigid as it is in elasmobranchs (p. 160). There is no communication
between the pericardial and peritoneal chambers. There is a vagal
cardiac depressor nerve, but no sympathetic nerve to the heart.

There is a well-developed lymphatic system beneath the skin and
in the muscles and viscera. Lymphoid tissue is abundant in various
organs but there are no lymph-nodes along the vessels. There is a
large spleen concerned with haemopoiesis, which also proceeds in the
kidneys. The red cells are smaller in bony fishes (8-10 ix) than in
elasmobranchs (up to 20 /z). A continuous series of white cells is
present and acidic and basic granules may occur in the same cell.

9. Urinogenital system and osmoregulation

The kidneys are mesonephric in the adult and consist of an elon-
gated brown mass above the air-bladder. The ducts of the two kidneys
join posteriorly and are swollen to form a bladder which, being meso-
dermal, must be distinguished from the endodermal cloacal bladder
of tetrapods. The urinary duct opens separately behind the anus,
there being no common cloaca.

Nitrogenous elimination is a function mainly of the gills, which
excrete as ammonia and urea more than six times as much nitrogen as
the kidneys. The latter excrete creatine, uric acid, and the weak base
trimethylamine oxide, which is present in large amounts in the blood
of marine teleosts.

One of the most striking features of the life of bony fishes is that
they occur both in fresh water and the sea, and many, such as the
trout itself, can move from one to the other. It is supposed by some
that the earliest gnathostomes were freshwater animals (p. 187), and
the bony fishes might be said to show evidence of this in that the
concentration of salt in their blood is always less than in the sea, in the
neighbourhood of 1-4 per cent. NaCl against 3-5 per cent, outside.

vii. 9 BLOOD OF TELEOSTS 203

In fishes in fresh water the blood is more dilute, about o-6 per cent.
NaCl, but is, of course, more concentrated than the surrounding
medium, which contains only traces of inorganic ions. Freshwater
fishes are able to take up salts from the water through the gill surfaces.
The kidney apparatus, with its filtration system of glomeruli and
tubules for salt reabsorption, was probably developed for life in fresh
water and still serves in this way in the freshwater forms. Various
special devices are adopted in fresh water for minimizing the tendency

Fig. 122. Diagram of the branchial circulation of a teleostean fish.
ab. artery to air-bladder; a/ 3-6 , four afferent vessels from ventral aorta; ca. carotid artery;
cc. circulus cephalicus; cl. coeliac artery; d. ductus Cuvieri; da. dorsal aorta; ef 3 . efferent
vessel of first branchial arch; ep. epibranchial artery; ha. hyoidean artery (afferent vessel of
pseudobranch); hp. hepatic vein; ht. heart; mis. mesenteric artery; oa. ophthalmic artery
(efferent vessel of pseudobranch); ps. pseudobranch (hyoidean gill, possibly with spiracular
gill); s. position of spiracle (closed); va. ventral aorta; I-V. five branchial slits. (From
Goodrich, Vertebrata, A. & C. Black, Ltd., after Parker.)

to gain water and lose salt. The skin is little vascularized and probably
makes an almost waterproof layer. The production of mucus assists
in this waterproofing, and abundant mucus is secreted when an eel is
transferred from salt to fresh water: the full change cannot be made
suddenly without killing the fish.

In marine teleosts the problem is the opposite one of keeping water
in, or keeping out salt. The usual kidney mechanism is clearly ill
suited for this and it is found that the glomeruli are few, or often
completely absent from the kidneys. This no doubt reduces the loss
of water, but is not enough by itself to solve the problem, which is
met by taking in water and salts and excreting the salts. For this
purpose special chloride-secreting cells are present in the gills and it
has been shown that the amount of oxygen they use, and hence the
work they do in diluting the blood, is proportional to the difference of
concentration between the inside and the outside. A marine fish is
able to drink and absorb sea water in spite of the fact that this is more

204

BONY FISHES

vir. 9-

concentrated than its blood. The chloride-secreting cells dispose of
the excess salts. It remains to explain the means by which a solution
passes against the osmotic gradient from the cavity of the gut to the
blood; the membranes here must have some special properties of
which we are ignorant. Sodium and chloride enter with the water but
magnesium is excluded and may be precipitated in the intestine.

The genital system is nearly completely separated from the excre-
tory in both sexes. The testes (soft roes) are a large pair of sacs opening

into the base of the urinary
ducts. The ovaries (hard roes)
are also elongated in the trout
and the eggs are shed free into
the coelom (Fig. 123) and
passed to the exterior by
abdominal pores. This condi-
tion is unusual among teleosts,
in most the ovaries are closed
sacs, continuous with the ovi-
ducts.

Fertilization is external and
the eggs of the trout are shed
in small pits or depressions in
the sand; being sticky, they
become attached to small
stones. The eggs are very
yolky and cleavage is therefore only partial, forming a cap of cells,
the blastoderm, which eventually differentiates into the embryo.
After hatching, the young fish may still carry the yolk sac and
obtain food from it for some time, while beginning to eat the small
crustaceans and other animals that are its first food.

10. Races of trout and salmon and their breeding habits

There is considerable confusion about the various races of trout
and their allies the salmon. In both trout and salmon the adult
originally spent the great part of its life in the sea but returned to the
rivers to breed. Trout and salmon that do this are still abundant on
the West Atlantic coasts and ascend all suitable rivers to breed, the
process being known as the 'run'. But the trout has produced many
races of purely fluviatile animals, living either in lakes (where they often
become very large) or rivers, and never returning to the sea to breed.
These freshwater races differ in small points from each other and are

Fig. 123. Ovaries and kidneys of A, typical

teleostean fish, B, trout and some other fishes

where the eggs are shed into the coelom.

(From Norman, after Rey.)

VII. IO

LIFE CYCLE OF SALMO

205

given various common names (phinock, Severn, Loch Leven trout,
brook trout, &c). There can be no doubt that interesting genetic
differences between these forms exist, but they have not yet been
fully studied. The salmon are much less prone to form purely fresh-
water races, though such are known.

During the breeding-season characteristic changes take place in the
fishes and differences between the sexes appear. In the salmon the
jaws become long, thin, and hooked, especially in the male. The
animals make pairs and the males fight with others that approach the
female. As the gonads ripen, the other
parts of the fish, which were well supplied
with fat at the beginning of the run,
become progressively more watery.
Finally, spawning takes place, the female
laying the eggs in a shallow trough (redd),
which she has 'cut' in the gravel by move-
ments of her tail, while the male sheds
sperms over them. She then covers the
eggs with gravel by further cutting move-
ments. The young male salmon (parr),
which have not yet been to the sea, may
become sexually mature. They accompany
the fully grown fish, hanging around the
cloacal region and shedding their sperms
at the same time as the large male. It is possible that this develop-
ment of a kind of third sex serves to increase the variability of the
population. The spent parr eat some of the eggs and they then proceed
to grow, migrate to the sea, and return later.

Male trout will follow a spawning salmon and fertilize her eggs if
her own male is not looking. Hybrids formed in this way can develop,
but are said to be less fertile than the normal types; indeed, the males
are wholly sterile.

After fertilization the salmon are very exhausted (known as kelts) ;
the males seldom return to the sea. The females, however, may recover
and after a period in the sea return to breed again, and this process
may be repeated several times.

Very young trout or salmon are known as alevins or fry and remain
mostly among the stones (Fig. 124). When they emerge they are called
parr and have a number of characteristic parr-marks along their sides.
After two to four years spent as parr in fresh water salmon acquire a
silver colour and pass to the sea as smolts. Young salmon returning for

Fig. 124. Three stages in the

development of the salmon.

I and II are alevins; III, parr.

(From Norman.)

206

BONY FISHES

the first time to breed are called maidens. If they have spent only one
and a half years in the sea they are called grilse and may then return
to the sea as kelts. Others ascend for the first time after three years
or more at sea.

It is well established that salmon nearly always return to breed in
the river in which they were born, and it is certain that they may
journey for considerable distances in the sea. The mechanisms by
which these migrations are initiated and guided are only partly known.

Fig. 125. Pituitary gland of the primitive teleost Elops, showing the persistent
Rathke's pouch in the form of a hollow bucco-hypophysial canal, piercing the

parasphenoid bone.

ah. adenohypophysis ; b.h.c. bucco-hypophysial canal; h.v. blood-vessel; c. continuation with

pharynx; i. infundibulum; n.h. neurohypophysis;/)^, parasphenoid.

(After Olsson.)

They probably involve endocrine changes, for example the thyroid
is very active in the smolt as they begin to migrate. The return to the
home river may be a result of olfactory conditioning (see p. 221).

11. Endocrine glands of bony fishes

The pituitary gland occupies the same central part in the endocrine
signalling system that it has in mammals. Neural and glandular
regions are present and the adenohypophysis has three parts, the
two more posterior corresponding to the mammalian intermediate and
anterior lobes. The most anterior glandular region may be comparable
to the pars tuberalis. Experiments by removal and injection have
shown that the middle portion produces hormones that stimulate
growth, the gonads, the thyroid, adrenal, and probably the pancreas.
The posterior lobe produces a melanophore-dispersing hormone

ENDOCRINE GLANDS

207

(p. 260) and there may be a melanophore-concentrating one in the
anterior lobe. Oxytocin and vasopressin are present but there is no
evidence that excretion is controlled by the pituitary.

The thyroid tissue is not aggregated into a compact gland but forms
scattered masses along the ventral aorta. Its hormones appear to be

ns.a.

Fig. 126. Urohypophysis of A, eel; b, loach (Misgurnus); c, the same in a loach

after sectioning the spinal cord and injecting hypertonic saline.

b. blood-vessels; ep. ependyma;//. filum terminate; /;/. lumps of secretion (? 'Herring bodies');

tie. nerve endings; ns.a. neurosecretory axon; ns.c. neurosecretory cells; s.d. storage depot of

neurosecretion. (After F.nami, N., in Symposium on Comparative Endocrinology. Wiley, New

York.)

identical with those of mammals, including mono- and di-iodotyrosine
and thyroxin. Thyroid follicles are often found in the kidneys, heart,
eye, and elsewhere in the body of fishes, especially those deprived of
iodine.

The suprarenal and interrenal tissues are partly associated in masses
around the thickened walls of the posterior cardinal veins. Because of
the difficulty of isolating these tissues there is little information as to
their function. The corpuscles of Stannius are groups of gland cells
dorsal to the kidnevs, they have been held to be related to the adrenals,
but their nature is still uncertain.

208

BONY FISHES

The ultimobranchial gland is a mass of cells developed from the
last branchial pouch and perhaps related to the parathyroids.

The hormone rennin, which raises the blood pressure, is said to be
present in freshwater teleosts, with their high glomerular filtration,
but not in marine ones.

The gonads produce steroid hormones as in elasmobranchs (p.
167). The secondary sex characters depend upon their presence, thus

ns. c.

n.e

Fig. 127. Comparison of pattern of organization of the caudal neurosecretory
system (b) with the hypothalamo-hypophysial system (a).

ah. adenohypophysis; b.v. blood-vessels; c.c. central canal; /.i. filum terminale; h. 'Herring
bodies', neurosecretory products; n. neurohypophysis; n.e. nerve endings; ns.c. neurosecre-
tory cells; o.c. optic chiasma; p. pituicytes; p.v. hypophysial portal vessels; r.f. Reissner's fibre;
11. urohypophysis; v. vtntricle. (After Enami, N., in Symposium on Comparative Endocrinology.

Wiley, New York.)

the gonopodium of the male of viviparous fishes (p. 267) is developed
if sex hormone is added to the water.

At the hind end of the spinal cord of fishes is a small lump consisting
of masses of secretion produced by neurosecretory cells of the spinal
cord and hence called the urohypophysis (Figs. 126 and 127). In
function it appears to be connected with salt regulation; injection of
hypertonic NaCl produces hypersecretion, the products accumulating
at the cut surface if the cord has been severed. Injection of extracts
produces changes in the sodium content of the fish and also changes

VII. 12

FOREBRAIN

209

in buoyancy, perhaps due to an influence on the carbonic anhydrase
of the gas bladder.

12. Brain of bony fishes

The brain of bony fishes is built on the same general functional and
structural plan as that of elasmobranchs, namely, the development of a
number of separate centres, one concerned with each of the main
receptor systems. The forebrain is often large, but it is characterized

chiasma
opticum

rec. pr.

Fig. 127 {a). Cross-section of the forebrain of the cod.
lat.tr. and tn.tr. lateral and medial tracts between olfactory region and hypothalamus; hyp.
hypothalamus; m. membranous roof of forebrain; n.mag. nucleus magnocellularis preopticus;
n.opt. optic tracts (that on the right has atrophied in this specimen) ; rec. pr. preoptic recess ;
str. hind end of striatum; thai, thalamus; 3rd v. third ventricle. (From Kappers, Huber,

and Crosby.)

by great development of its ventral regions (the 'corpus striatum'), the
roof being wholly membranous (Figs. 127 (a), 128). This condition is
known as 'eversion' and is the very opposite to the inverted or thick-
roofed forebrains that are found in the lung-fishes, close to the line
of tetrapod descent (p. 278). The whole of this forebrain is reached by
olfactory fibres, and there is little evidence that fibres from other
receptor centres reach forward to it; it is mostly a smell brain.
Extirpation of the telencephalon from various teleosts has not
produced changes in locomotion, balance, or vision; there may be
slight changes in general activity and social behaviour. No movements
have been seen following electrical stimulation of it.

The diencephalon is not large, since most of the optic fibres end
not here, but in the midbrain. The roof is everted to form a pineal
body, and this and other parts of the diencephalon may contain

210 BONY FISHES vn. 12

receptors sensitive to light. The minnow Phoxinus has a transparent
patch on the head in this region, and it has been found possible to
train the fish to give appropriate responses to changes of illumination
even after removal of the paired eyes and the pineal body. Evidently
there are light-sensitive cells in other parts of the walls of the dien-
cephalon, besides those that become evaginated to form the eyes.
Experiments on lampreys also showed the presence of such cells
(p. 105). The hypothalamus is well developed and receives large tracts
from the forebrain. Below and behind it is a large saccus vasculosus
in some forms (p. 169).

The midbrain is often the largest part of the brain. The cells spread
out over its roof (tectum opticum) are not all collected round the
ventricle but have migrated away to make an elaborately layered
system. Into this midbrain cortex there pass not only the great optic
tracts but also ascending tracts from the sensory regions of the spinal
cord, lateral line system, gustatory systems, and cerebellum. Large
motor tracts pass back towards the spinal cord; the details of their
endings have not been traced, but they certainly exercise control over
motor functions. Electrical stimulation of the optic lobes produces
well-coordinated movements of local groups of muscles, for instance
those of the eyes or fins. It can hardly be doubted that this well-
developed midbrain apparatus thus controls much of the behaviour of
the fish and is able to mediate quite elaborate acts of learning and
other forms of more complex behaviour. After removal of the tectum
of one side a minnow is blind in the opposite eye. Each part of the
retina is mapped on to a distinct area of the tectum and if the optic
tract is cut and allowed to regenerate this projection is exactly replaced.
When a goldfish is trained to respond to some visual stimulus the
learning process occurs in the midbrain and continues unaffected after
removal of the forebrain. Conversely, olfactory learning takes place
in the latter and is undisturbed by injury to the tectum opticum.

The base of the midbrain (tegmentum) contains motor centres.
Electrical stimulation here produces abrupt and massive responses of
the locomotor apparatus, very different from the sequences of co-
ordinated movements that appear after stimulation of the roof of the
tectum.

The cerebellum is very large in teleosts, especially in the more
active swimmers, and a forwardly directed lobe of it, the valvula
cerebelli, extends under the midbrain. Various disorders of movement
have been reported after removal of the cerebellum, such as swaying
when moving quickly. Presumably it plays an important part, as in

HKA1N OF TELEOSTS

Fie. 128. Transverse sections of forcbrain in various vertebrates to show the condition

of inversion (thick roof) in A, n, and c and eversion (thin roof) in D, E, and F.

A, lamprey; B, frog; C, chelonian; D, chimaera; E. sturgeon; F, teleostean; pall, pallium;

sep. septum; str. striatum. (From Kappers, Huber, and Crosby.)

Fig. 129. Sagittal section of brain of the gurnard, showing the swellings in the

spinal cord at the point of entry of the nerves from the fin.

C. cerebral hemisphere; ce. cerebellum; hy. hypothalamus; in. midbrain; no. swellings of

spinal cord; v. valvula. (From Scharrer, Z. verg. Physiol. 22.)

other vertebrates, in producing precise and correctly timed movements.
It is enormous in the Mormyridae, where it may assist in direction-
finding by electrical pulses (p. 253), perhaps acting as a timing device.
The medulla oblongata is also well developed, having special lobes
connected with the entry of the lateral line nerves and gustatory fibres
of the cranial nerves. In the gurnard, Trigla, there are chemical
receptors in the elongated fins. These are innervated from spinal
nerves, and there are swellings of the dorsal part of the spinal cord at
the points where these nerves enter (Fig. 129).

212 BONY FISHES vn. 13-

13. Receptors for life in the water

The features of the environment that are relevant for life are very
different in air and water. Man is so well used to the air that it is not
easy to appreciate fully the conditions underwater, where changes of
illumination, though obviously important, provide less detailed evid-
ence of the sequence of distant events than they do in air. We can
say that light carries less information for a fish; to put it in another
way, fewer distinct choices between alternative behaviour pathways
are made on the basis of visual clues by a fish than by a man.

On the other hand, the water around the fish provides mechanical
stimuli both at low and high frequency that are more closely related
to distant events than is generally true in air. Both hearing and touch
are of great importance in the water and the lateral line system pro-
vides a system of 'distant touch' that is perhaps wholly outside our
experience. Localization of distant objects by such a sense, perhaps
assisted by echo-location by water movements, provides the fish with
many relevant clues. It is interesting that these receptors are connected
with a very large cerebellar system, perhaps concerned with measur-
ing time differences.

Chemical changes in the water also provide much information and
both taste and smell are well developed. That smell is analysed by a
distinct system in the forebrain, not directly related to the cerebellar
system, is one of the fundamental principles of control of vertebrate
behaviour. Distant chemical changes provide the first clue to the
presence of food, a mate, or an enemy, whereas the detailed finding
of these involves eyes, ears, touch, and an accurate timing system.
There thus arises the distinction between the systems for initiation of
action in the forebrain ('emotive') and for its fulfilment (executive)
by centres farther back.

14. Eyes

An animal provided with suitable receptors can obtain much
information about the environment from the changes in illumination.
Control of the whole physiology to follow the rhythm of day and night
may have been the original reason for the development of photo-
sensitivity in the diencephalon (see p. 105). At the stage of evolution
reached by teleosts information is gained from the fact that light
varies in frequency (colour) and intensity (brightness) and that it is
reflected from many substances, revealing their movement and shape.
The greatest sensitivity of the fish eye is in the yellow-green, which

vii. 14 EYE OF TELEOSTS 213

is the wavelength that penetrates farthest into the water. In order to
extract the maximum of information at high as well as low intensities
it is necessary to adjust the sensitivity, and hence the signal/noise
ratio. For this purpose teleosts have developed retinas with distinct
rods, cones, and twin-cones and in some there is a fovea composed of
numerous thin cones (e.g. in Blennius). The pupil usually varies little
in diameter, and adjustment of sensitivity is by migration of pigment

scleral cartilage

epichorioKJal lymph space

choriad
'glond

Fig. 130. Diagrammatic vertical section of a typical teleostean eye. Not all the structures
here shown are found in all species. (From Walls, The Vertebrate Eye.)

between the receptors and contraction of a 'myoid' segment of the
latter. In bright light the pigment expands, the cones contract for-
ward, towards the light and the rods contract back, beneath the pig-
ment. These photo-mechanical changes thus serve the same end as
changes of pupil diameter in other vertebrates.

The photochemical change in the rods of marine fishes is the same
as that of land vertebrates, namely the breakdown of the rose-
coloured 'visual purple' (rhodopsin) first to the yellow retinene and
then to colourless vitamin A v In freshwater fishes there is a different
pigment porphyropsin, or visual violet, which breaks down to vita-
min A 2 . Intermediates between these may be found.

In all fishes there is a very large, dense, spherical lens, to which is
attached a retractor muscle (campanula Halleri) inserted on to a fal-
ciform ligament, which occupies the persistent choroidal fissure in the
retina (Fig. 130). The eye is usually said to be myopic at rest and to be
accommodated for distant vision by pulling the lens nearer to the

214 BONY FISHES vn. 14

retina. However, this has recently been disputed by Verrier, who
denies that the campanula is muscular and believes the eye to be
hypermetropic at rest and accommodated, if at all, by fibres of the
ciliary body, as in other vertebrates. It may be that the fixed focus is
already sufficiently deep and the campanula perhaps serves mainly
to steady the lens.

It is unwise, however, to generalize about teleostean eyes, for they
are very varied. Whereas the trout, like most, has a round pupil,
which varies little if at all in size, other fishes, whose eyes are more
exposed to light from above, have a more mobile iris. In flat-fishes
and the angler-fishes, such as Lophius, and the Mediterranean
Uranoscopus, the star gazer, the iris has an 'operculum' and is very
muscular; its movements are controlled by nerves and not, as in
selachians, by the direct effect of light. The sympathetic system sends
branches into the head in these animals (Fig. 138) and its fibres cause
contraction of the sphincter of the iris, whereas fibres in the oculo-
motor nerve cause contraction of the dilatator, the opposite arrange-
ment to that in mammals. In the eel the pupil is also capable of wide
changes of diameter, but here the control is mainly by the direct
response of the circular sphincter iridis muscle to light incident upon
it. The pupil of the isolated eye of an eel closes when illuminated and
reopens again in darkness (Fig. 131). Presumably because of its lack
of nervous control this iris is not affected by many of the usual
'autonomic' drugs. For instance, closure will occur in the presence of
atropine and the dark-adapted pupil remains unchanged when placed
in a solution as strong as 1 per cent, pilocarpine, but then closes
immediately on illumination (Fig. 132). The isolated pupil of Urano-
scopus, however, closes when pilocarpine is applied (Fig. 133), and
in this case the sphincter muscle is innervated by sympathetic nerve-
fibres. Adrenaline also causes the sphincter to contract and acetyl
choline in moderate concentrations causes dilatation

The eyes may be small or absent in fishes living in caves, muddy
waters, or the deep sea. In this last habitat, however, many have ex-
ceptionally large eyes, with, apparently, high acuity as well as sensi-
tivity. They may be elongated ('telescopic') and with large binocular
fields and a fovea of 'rods'. In Bathylagus the rods reach a density
of 800,000 mm 2 and are arranged in six superimposed layers, which
presumably come into action successively as an object approaches.
The cells of the deeper layers are less closely packed.

The tropical fish Anableps lives with the head half out of water and
the eyes are adapted for use in both media. The upper part of the

(215)

Red

White light

Red light

8
7

2
1

i i i

Time,

minutes

Fig. 131. Closure of the pupil of the isolated eel's eye, followed by plotting the move-
ment of its margin with a camera lucida. The movements are shown magnified 54 X ,

Time in minutes.

U-

2-35

Ringer

2;Z0

-2-05
-1-90
1-75
1-60
145
1-30
1-15

Acetul choline . . , L ■■
Vmnnnnn Acetylcholine

1/100.000 Atropine 7100,000

Vl .000.000

Red light

White

Red

20 11

Time, minutes

Fig. 132. Changes of diameter of isolated eel's iris in Ringer's solution with the

addition of various drugs. Acetyl choline produces some closure, atropine some

opening. Light still produces closure after application of atropine.

Pilocarpine

Fig. 133. Movements of margin of pupil in isolated iris of Uranoscopus in isotonic

solution. Pilocarpine produces closure and atropine opening of this pupil whose

sphincter muscle is innervated by sympathetic nerve-fibres.

(From Young, Proc. Roy. Soc. B. 107.)

2l6

BONY FISHES

vii. 14-

cornea is thickened, the iris provides two pupils, the lens is pear-
shaped, and there are two retinas in each eye.

15. Ear and hearing of fishes

The ear provides receptors that ensure the maintenance of a correct
position of the fish in relation to gravity and to angular accelerations.
In addition, in many species it serves for hearing. The inner ear is
completely enclosed in the otic bones. There is a perilymphatic space
only in those species that hear well.

ant.

Ns Sag. S. L.

Fig. 134. Diagram of ear of the minnow Phoxinus.

Ast. asteriscus; L. lagena; N.I., N.s. nerves of lagena and saccule;

S. saccule; Sag. sagitta; U. utricle. (From V. Frisch, Z. vergl.

Physiol. 25.)

Each ear sac is subdivided into three semicircular canals and three
other chambers, the utriculus, sacculus, and lagena (Fig. 134). In
each chamber is carried an ear stone (otolith) and these are given
special names, the lapillus, sagitta, and asteriscus, occupying the above
three chambers respectively.

The sensitive macula of the utricle lies horizontally, with the
lapillus resting upon it, whereas the maculae of the saccule and lagena
are vertical. These receptors with otoliths have double or triple
functions. At rest they act as static receptors, signalling the position
of the fish in relation to gravity and setting the fins and eyes in appro-
priate positions. In movement, together with the semicircular canals,
they signal angular accelerations, initiating compensatory movements.
Thirdly, some of the otolith organs respond to sonic vibrations.

In the fishes that hear well there is a connexion between the air
bladder and the ear. This may be either direct, by means of a sac
extending forwards (in Clupeidae and others) or indirectly by a chain
of modified vertebrae, the Weberian ossicles (Fig. 135). This latter
arrangement is found in the freshwater Ostariophysi, which hear

vii. 15 HEARING OF FISHES 217

particularly well. In these fishes the receptors are in the inferior part
of the ear (saccule and lagena, Fig. 134). The sagitta carries a special
wing projecting into the cavity and is so suspended as to serve to
amplify vibrations. Near to it is
a thin portion of the wall of the
sac, which would favour the
passage of variations of pressure
transmitted to the endolymph by
the ossicles.

These Ostariophysi respond to
sounds between about 60-6,000
vibrations/sec. After removal of
the pars inferior responses con-
tinue only up to 120/sec. If the
air bladder is punctured a min-
now can still respond, but only
up to 3,000/sec and with a sen-
sitivity diminished by more than
fifty times.

Minnows can be trained to
discriminate between warbled
notes separated by I tone. Non-
ostariophyse fishes have mostly
a much lower upper limit of
hearing and lower capacity for
discrimination. The Mormyridae
(p. 254), however, approach the
minnows in this respect and here
there is a special isolated portion
of the air bladder within the otic
bone.

In the best cases the sense of
hearing of fishes thus approaches
that of man, in spite of the
absence of a coiled cochlea and

basilar membrane with fibres of different lengths. Clearly the discrimi-
nation of tones cannot here depend upon differential resonance as the
theory of Helmholtz requires. In spite of the considerable powers
of pitch discrimination there is little evidence of capacity to localize
sounds except when they are loud and near.

Sch.

Fig. 135. Position of ear in Ostariophysi

and its relation to the Weberian ossicles,

which are shown in black.

C.tr. transverse canal between the two sacculi;
//. brain; /. 'incus'; L. lagena; M. 'malleus';
S. sacculus; Sch. swim-bladder; S.i. sinus impar
(perilymphatic space); St. 'stapes'; U. utriculus.
(From V. Frisch.)

218 BONY FISHES vii. 16-

16. Sound production in fishes

A surprisingly large number of fishes can produce sounds audible
to ourselves, and these noises are used by the fishes either for shoaling,
or to bring the sexes together, or to warn or startle enemies. Some fish
may use the sounds they produce for echo-location. Among the loudest
of the sounds is that produced by the drum-fish (Pogonias) of the
Eastern Atlantic. The 'whistling' and other noises of the 'maigre'
(Sciaend) are supposed to be the origin of the song of the Sirens, since
they can easily be heard above the water. In both these fishes the
sounds are made mostly if not wholly in the breeding season. In
others, such as siluroids and Diodon, the noise is associated with the
presence of spines and may be a warning. In Congiopodas the nerves
that innervate the muscles of sound production also supply muscles
that raise the spines (Packard).

The mechanism for sound production is very varied, involving
either stridulation by the vertebrae (some siluroids), operculum
(Cottus, the bull-head), pectoral girdle (trigger-fishes), teeth (some
mackerel and sun-fish), or phonation by the air bladder. The latter
may be involved either by its use for 'breathing' sounds in physosto-
matous forms (p. 261) or as a resonator. Noise production is common
in some families (Triglidae, Sciaenidae, Siluridae) but almost absent
from others. The advantages to be obtained from sound production
underwater have led to parallel evolution of similar mechanisms in
several different groups.

17. The lateral line organs of fishes

The lateral line organs occur partly as rows of distinct pits, partly
in canals that communicate with the surface through pores in the
scales. Besides the main canal running down the body and served
by the lateral line branch of the tenth cranial nerve, there are also
lines following a definite pattern on the head, namely, supra- and
sub-orbital lines, a line on the lower jaw, and a temporal line across
the back of the skull. The canals on the head are innervated mainly
from the seventh, partly from the ninth cranial nerve. The nerve-
fibres enter the very large acoustico-lateral centres of the medulla and
valvula cerebelli.

Fishes possess the capacity to react to an object moving some dis-
tance away in the water ('distant touch sense') and this is reduced or
absent after section of the lateral line nerve. Presumably the moving
object sets up currents in the water, which move the fluid (or mucus)
in the canals. It has also been suggested that the canals serve to record

vii. 17

FUNCTION OF LATERAL LINE

219

displacements produced by the swimming movements of the fish
itself, but this has not been proved. Fishes deprived of the lateral
line show no muscular incoordination, although if blind they collide
frequently with solid objects. It has often been suggested that these
organs serve for hearing, perhaps at low frequencies, but this is
probably not so.

Fig. 136. Responses of a single end organ in a lateral canal of a ray, shown with an
oscillograph after amplification. Time signal 10 sec. intervals. The movements of
the continuous white line show A, the beginning of a headward flow, increasing the
frequency of discharge; B, the end of this flow; c, return of spontaneous discharge
after an interval of 28 sec; D, spontaneous discharge 60 sec. later; E, beginning of
a tailward perfusion, inhibiting the discharge; F, the end of this perfusion; G, the
spontaneous discharge 10 sec. later. (From Sand, Proc. Roy. Soc. B. 123.)

Study of the electrical activities of these organs in rays has shown
that many of them discharge impulses all the time, even when not
under the influence of any external stimulation (Fig. 136). By passing
currents of water along the tubes Sand showed that a tailward flow
checks and a headward flow accelerates this 'spontaneous' discharge of
impulses. Such changes in the streams of impulses arriving at the
brain could, no doubt, form the basis for initiation of movements of

220

BONY FISHES

vii. 17-

the fish. This, however, still leaves open the question of what agency
initiates movement of the fluid in the canals during life. It has been
shown that when small streams of water are directed against the side
of the tail some fish make escaping movements, but that these no
longer appear when the lateral line nerve has been cut. The lateral
line organs thus provide signals when agitation of the water causes
pressure changes. In fact they provide the animal with a kind of
water touch, though it is not certain whether this is their only func-

/^v Lat.d.
gust.

max

Lat.v.
pelv. pect.

Fig. 137. Dissection of whiting to show the cranial nerves, and especially the
nerves for the taste-buds.

an. anal fin; gust, gustatory branch of facial; lat.d. and lat.v. dorsal and ventral lateral line

nerves of vagus; mand. and max. mandibular and maxillary divisions of trigeminal; op.

ophthalmic; pect. pectoral fin; pelv. pelvic fin; VII, hyomandibular branch of facial; IX,

glossopharyngeal; X.visc. visceral branch of vagus.

tion. Why this type of receptor should need such a peculiar apparatus
of canals, rather than a system of nerve-fibres in the skin, innervated
by the spinal dorsal roots, is not clear, nor do we know the significance
of the pattern of lines on the head. The lateral line system must cer-
tainly be of great importance in aquatic life, for it is found in all types
of fishes and also in the early Amphibia and in the aquatic larvae of
modern members of that group. The distant touch receptors could
obviously be used in many ways, not only to locate moving objects
and water currents but to serve for echo-location, by computing the
time relation of reflected waves set up by the fish itself.

18. Chemoreceptors. Taste and smell

As in all vertebrates, there are two separate chemical senses, taste
and smell. The former serves mainly to produce appropriate reactions
to food near the body, such as snapping, swallowing, or movements
of rejection. Smell, on the other hand, is a 'distance sense', by which
the whole animal is steered. The distinction between the two types
of receptor is somewhat obscured in bony fishes by the fact that taste-
buds are not restricted as they are in mammals to the tongue and

vii. i8 TASTE AND SMELL 221

pharynx but may occur on the whiskers and all over the body. They
are innervated by branches of the seventh, ninth, and tenth cranial
nerves, which may reach far backwards (Fig. 137). In some species it
has been shown that the fish is able to turn and snap at a piece of food
placed near the tail. This power is lost if the branches from the cranial
nerves are cut. In mammals taste-buds serve to discriminate only four
qualities (salt, sour, bitter, and sweet), most of our so-called 'tasting'
being in reality the smelling of the food in the mouth. In fishes, also,
the four taste qualities are discriminated by the taste-bud system, and
it has been shown that the minnow (Phoxinus) continues to make such
discriminations after the forebrain has been removed. Other chemical
discriminations are made by the nose, however, and can only be
performed with an intact forebrain. Thus Phoxinus tastes and smells
the same classes of substances as man does. The taste-buds are
exceedingly sensitive, the threshold for sweet substances being 500
times and for salt 200 times lower than in man. On the other hand,
some substances that are very bitter for us produce little reaction in
Phoxinus.

In many fishes the nose is one of the chief receptors (macrosmatic).
There are two nostrils on each side, allowing for the sampling of a
stream of water (Fig. 119). The nose does not communicate with the
mouth, except in a few fishes that live buried in the sand (Astroscopus).
The sense of smell is used to find food and for recognition of the
sex of members of the same species. Minnows can be trained to give
distinct reactions to extracts made from the skin of other species of
fish living in fresh water. In the presence of 'alarm substances' pro-
duced by damaged skin of a member of the same species, minnows
(and other fishes) show a 'fright reaction', scattering and refusing food.
The state of development of the nose is very varied. It is large in
macrosmatic solitary predators such as Anguilla and in many schooling
species that also have well-developed eyes {Phoxinus, Gobio). Daylight
predators, on the other hand, are microsmatic (Esox, Gasterosteus).
Other evidence shows that fishes can discriminate between the smells
of water plants and between the waters of different streams. It is
likely that this provides part of the mechanism by which salmon
return to the stream in which they were born, having been conditioned
as fry to the smell of its water. It has been suggested that they might
be decoyed to return to a stream other than that where they were
hatched by conditioning them as fry to a substance such as morpholene
to which they have a high sensitivity although it is neither an attract-
ant nor repellant.

222

BONY FISHES

vii. 19-

Fig. 138. Diagram of ventral view of the
sympathetic system of the front part of the
body of Uranoscopus, showing the fibres
in the sympathetic and oculomotor that are
responsible for the light reflex.
(From Young.)

cil.brev. cil.long., short and long ciliary nerves;
cil.gn., ciliary ganglion; dors.r. dorsal root; dil.
dilatator muscle; hypo, hypoglossal; n.splanch.
splanchnic nerve; opt. optic nerve; p. pupil;
pal. VII, palatine branch of facial ; prof, profun-
dus; r.b. short root of ciliary ganglion; r.comm.
ramus communicans; r.l. long root of ciliary
ganglion; sph. sphincter muscle; ventr.r. ven-
tral root; 1II-X, cranial nerves with their
sympathetic ganglia (V.symp. &c.); VII hyo.
hyomandibular branch of facial; r— 4 sp.symp.
spinal sympathetic ganglia.

19. Touch

Touch is, of course, well
developed in fishes, and in many
species there are special sensory
filaments, which presumably serve
this sense. They are usually de-
veloped around the mouth, as in
the catfish; in other fishes they
are modifications of the fins, for
instance, the pectoral fins of
gurnards, which also contain
chemoreceptors.

20. Autonomic nervous system

The autonomic nervous system
of bony fishes is organized on a
plan rather different from that
both of elasmobranchs and of
land animals. There is a chain of
sympathetic ganglia, extending
from the level of the trigeminal
nerve backwards, a ganglion
being found in connexion with
each of the cranial dorsal roots
(Figs. 138 and 139). These gan-
glia do not receive pre-ganglionic
fibres from the segments in which
they lie, but by fibres that run out
in the ventral roots of the trunk
region and thence forwards in the
sympathetic chain. This emer-
gence of the pre-ganglionic fibres
for the head in the trunk region
recalls the arrangement in land
animals.

Each trunk sympathetic gan-
glion, besides receiving a white
ramus communicans of pre-gan-
glionic fibres from its spinal nerve,
also sends a grey ramus back to

VII. 20

AUTONOMIC NERVES OF TELEOSTS

223

that nerve, this ramus carrying post-ganglionic fibres to the skin.
Some of these fibres control the melanophores, causing them to
contract (p. 259). In elasmobranchs there are no grey rami communi-
cantes and no sympathetic system in the head (p. 173); the differences
between the two groups are therefore very striking.

HI prof Viymp

Fig. 139. Diagram of the autonomic nervous system of Uranoscopus seen from the side.

bl. mesonephric bladder; cil.gn. ciliary ganglion; dors, dorsal root; n.sph. nerve to anal
sphincter; n.spl. splanchnic nerve; prof, nervus ophthalmicus profundus; rad. brev. short
root of ciliary ganglion; r.comm. ramus communicans (including both white and grey fibres);
stan. 'corpuscle of Stannius' (adrenal cortical tissue?); ventr. ventral root; ///, oculomotor
nerve; V— X symp. sympathetic ganglia associated with the cranial nerves. (From Young,

Quart. J. Micr. Sci. 75.)

Fig. 140. Tracing of the contractions of a strip of the stomach muscle of the angler-
fish, Lophins, attached to a lever. Time in minutes. At A, faradic stimulation of the
vagus nerve. Drugs then added to the solution to make, at B acetyl choline 1/1,000,000;
at c acetyl choline 1/100,000; at D adrenaline 1/100,000.
(From Young, Proc. Roy. Soc. 120.)

Little is known about the parasympathetic system of bony fishes.
The oculomotor nerve carries fibres to the iris, which work in the
opposite direction to fibres from the sympathetic (p. 214). There is
also a well-developed vagal system, but so far as is known no para-
sympathetic fibres in other cranial nerves and probably no sacral
parasympathetic system. Electrical stimulation of the vagus nerve

224 BONY FISHES vn. 20-

produces movements of the stomach but not of the intestine; the
latter, however, shows movements when the splanchnic nerve is
stimulated. In most of the viscera acetyl choline causes initiation of

nnnnnnnnnnnnnnnnnnnnnnnnnnnnnnnr

11111111111J1I.

Fig. 141. Tracing of contractions of the muscle of the urinary bladder of Lopliius,

attached to a lever. At A, D, and F faradic stimulation of vesicular nerve. Drugs added

to make, at b acetyl choline 1/2,000,000; at c adrenaline 1/500,000; at E ergotoxine

1/50,000. Time, minutes. (From Young.)

Fig. 142. Tracing to show effect of atropine 1/50,000 added at A, on the contractions

of the bladder of Lophius produced by faradic stimulation of the vesicular sympathetic

nerve. Time, minutes. (From Young.)

rhythmic contractions and these are inhibited by adrenaline (Figs.
140 and 141). In Lophius this is true of the stomach, with motor-fibres
from the vagus, intestine, with sympathetic motor-fibres, and of the
muscles of the bladder, which contract on stimulation of the hinder
sympathetic ganglia. However, in the trout adrenaline causes contrac-
tion of the stomach (Burnstock, 1958). The effect of the nerves to the

vii. 21 BEHAVIOUR OF FISHES 225

bladder is prevented by atropine (Fig. 142) but not by ergotoxine
(Fig. 141), though the latter is the drug that in mammals often inhibits
sympathetic motor-fibres. In these fishes, therefore, it is not possible
to divide up the autonomic nervous system into sympathetic and
parasympathetic divisions by either anatomical, physiological, or
pharmacological criteria. Presumably the two 'antagonistic' systems
found in mammals are a late development, allowing for a delicate
balancing of activities for the maintenance of homeostasis.

21. Behaviour patterns of fishes

The well-developed receptors and brain of the teleostean fishes
constitute perhaps the most important of all factors in giving them

Fig. 143. The red belly of the stickleback releases attacking behaviour in other males

and following by females. Of the above models only the two on the left acted as

releasers. (From Tinbergen, Wilson Bulletin, 1948.)

their great success. Varied habits and quick actions enable the fish to
make full use of the possibilities provided by the special features of
their structure — the air bladder, mouth, and so on. The receptors and
brain make it possible for the fish to learn to react appropriately to
many features of its surroundings. Thus the eyes besides orientating
the fish to movements in the visual field allow the discrimination of
wavelengths and distinct reactions to differing shapes (see Bull, 1957).

The social behaviour of many species includes the development of
special 'releasers', shapes, colours, or postures that are displayed by
one individual and elicit specific reactions in another (Fig. 143).

There is no doubt that fishes possess great powers of learning.
They can form conditioned reflexes involving discrimination of tones,
also second-order conditioned reflexes, in which after the animal has
learnt to give a certain behaviour in response to a visual stimulus it is
then taught to associate the latter with an olfactory stimulus. There
are many other examples of such powers, but unfortunately we have
as yet little information as to the way in which they are brought about
by the brain. Nor have the naturalists provided us with very clear
examples of the use of these powers by fishes in nature. There are

226

BONY FISHES

VII. 21

many tales of carp coming to be fed at the ringing of a bell, and similar
powers of association must play a part in the life of fishes in more
natural situations. Bull has shown that fishes can be trained to dis-
criminate between very small differences of water flow, temperature,
salinity or pH, and no doubt it is by means of such powers that they
normally find a suitable habitat.

Fig. 144. Migrations of the eels. The European species (A. anguilld) occurs along the
coasts outlined with lines, the American species {A. rostrata) where there are dots.
The curved lines show where larvae of the lengths indicated (in millimetres) are taken.

(After Norman.)

The migrations of fishes have attracted much attention, but are
still imperfectly understood. They vary from the 'catadromous' down-
ward migration of young animals to the sea and the reverse 'anadro-
mous' movement to breed, to the astounding journeys of the eels,
3,000 miles westwards from Europe or eastwards from America to
their breeding-place in the Sargasso Sea (off Bermuda) and the return
of the elvers to the homes of their parents (Fig. 144). No one has yet
discovered the factors that direct these movements, currents may play
a part, but can hardly be the only influence. Indeed it has been
suggested that European eels never complete the journey but die in

vii. 21 MIGRATION OF EELS 227

their own continental waters. The populations of so-called European
eels {Anguilla anguilld) would then be maintained by reinforcements
of larvae of the American A. rostrata, the differences between the
two being due to temperature and other factors (Tucker, 1959).

Social behaviour is marked in many species and shoals of some
fishes may contain many thousands of individuals. The animals are
presumably kept together in most species by visual stimuli, though
sounds may play a part. Shoaling gives protection to small fishes, and
in some species the animals come together in shoals to breed (her-
rings). There may also be some advantage for the finding of suitable
feeding conditions, but on all these points we can do little more than
speculate and hope for further information.

VIII

THE EVOLUTION OF BONY FISHES

1 . Classification

Class Actinopterygii
Superorder i. Chondrostei

Order i. Palaeoniscoidei. Devonian-Recent

*Cheirolepis; *Palaeoniscus; * Amphicentrum; *Platysomus,
*Dorypterus ; *Cleithrolepis; *Tarrasius; Polypterus, bichir
Order 2. Acipenseroidei. Jurassic-Recent

*Chondrosteus; Acipenser, sturgeon; Polyodon, paddle-fish
Order 3. Subholostei. Triassic-Jurassic
*Ptyeholepis
Superorder 2. Holostei. Triassic-Recent

*Acentrophorus; *Lepidotes; *Dapcdius; *Microdon; Amia,
bowfin; Lepisosteus, gar-pike
Superorder 3. Teleostei. Jurassic-Recent
Order 1. Isospondyli

*LeptoIepis; *Portheus; Clupea, herring; Salmo, trout
Order 2. Ostariophysi

Cyprinus, carp; Tinea, tench; Silurus, catfish
Order 3. Apodes

Angnilla, eel; Conger, conger eel
Order 4. Mesichthyes

Esox, pike ; Belone; Exoeoetus, flying fish ; Gasterostens, stickle-
back; Syngnathns, pipe-fish; Hippoeampus, seahorse
Order 5. Acanthopterygii

*HopIopteryx; Zens, John Dory; Perca, perch; Labrus, wrasse;
Uranoscopns, star gazer; Blennins, blenny; Gadus, whiting;
Pleuronectes, plaice; Solea, sole; Lophius, angler-fish

2. Order 1. Palaeoniscoidei

The actinopterygian stock has been distinct since Devonian times.
The early representatives lacked many of the specializations that we
find in the successful bony fishes today and showed features of simi-
larity to the Crossopterygii. These Devonian Actinopterygii had not
yet acquired the striking signs of full mastery of the waters, which are
so characteristic of the group today. They resembled their ancestors
the placoderms and their cousins the crossopterygians in being rather

VIII. 2

PALAEONISCIDS 229

clumsy, heavily armoured creatures. From this early type many lines
have been derived and can be followed with some completeness to
their extinction or modern descendants. Various classifications have
been suggested. The one used here is simple but for that very reason
obscures the multiplicity of parallel lines. A recent classification
recognizes fifty-two orders of Actinopterygii (Grasse).

Fig. 145. Scales of some early fishes.
A, hypothetical condition with denticle-like substance (d.) attached to a basal bony plate lying
in the connective tissue (ct:)\ B, 'cosmoid' scale of early crossopterygians, showing the cosmine
layer (co.) ; epidermis (ep.) ; vascular canals (hv.) and underlying 'isopedin' {is.); C, palaeoniscoid
scale with layers of 'ganoin' (ga.); d, lepidosteoid scale of the gar-fish with tubules (/.). (From
Goodrich, Vertebrata, A. & C. Black, Ltd.)

The Devonian and Carboniferous forms are grouped together in
the order Palaeoniscoidei, and animals of similar type survive today
as Polypterus, the bichir of African rivers, which though showing some
specializations remains in its general organization near the palaeoniscid
level.

A typical Palaeozoic palaeoniscid such as *Cheirolepis was a long-
bodied creature (Figs. 146 and 147) with a heterocercal tail, single
dorsal fin, and pelvic fins placed far back on the body. The pectoral
and pelvic fins had broad bases and the radials fanned out from a small
muscular lobe, present in all early actinopterygians but lost in later
forms. The body was covered with thick rhomboidal scales very
similar to those of acanthodians. They articulated by peg and socket
joints and have a structure known as palaeoniscoid (Fig. 145). The
scale is deeply embedded and grows by addition both to the bony or
isopedin portion and to the shiny surface-layer, the ganoin, which
thus becomes very thick. There is a middle layer of 'pulp' correspond-
ing to the cosmine layer of the cosmoid scale of Crossopterygii

230 BONY FISHES vm. a

(p. 269) and the two types have obvious similarities, though it is not
clear how they are related.

The skull was built on a distinctly different plan from that of
Crossopterygii, in that there was no joint such as was present in those
fishes to allow the front part to flex on the hind. The jaw support was
amphistylic, in the sense that the palatoquadrate was attached to the
neurocranium by a basal process, but the otic process did not reach
the skull and the hind end of the jaw was supported by the hyomandi-
bula. There were even more dermal bones than are found in modern
Actinopterygii, arranged so as to form a complete covering for the
chondrocranium and jaws. These bones were derived from the original
scaly covering of the head and the naming and comparing them with
the bones of other forms is a matter of some difficulty. Some of the
main bones resemble in appearance and shape those found in tetra-
pods, but there are others for which no such homologues can be
found, and sometimes there is considerable difficulty in recognizing
even the main outlines of the pattern. The problem is that we have
no rigid criterion by which to set about giving names to the skull
bones. No system yet discovered is wholly satisfactory, and we must
admit to insufficient knowledge of the factors that determine that
bone shall be laid down in certain areas and that sutures shall separate
these from each other. However, some of the dermal bones lie in
relation to the lateral line canals (or rows of neuromasts), which latter
may provide the stimulus to bone formation. The lines are remarkably
constant, perhaps because of their function in detecting water move-
ments in relation to swimming, and this is the factor that determines
the position of many of the bones. Others fill in the spaces between
(anamesic bones). Yet others may be differentiated in relation to the
teeth. However, the number of bones along any one line may vary
greatly even in one species (e.g. in Amid). The whole pattern is more
variable in fishes than in higher vertebrates, but it is usual to consider
that the bones of early Actinopterygii resemble those of Crossopterygii
and of the early amphibians (Fig. 194).

The roof of the skull usually shows a large pair of parietals between
the eyes, and post-parietals behind these. Between the parietals and
the nostrils there are frontal bones and the front of the head usually
also carries a number of rostral bones, not found in higher forms.
Behind the post-parietals in the midline is a series of extrascapular
bones.

The side of the skull of palaeoniscids is covered by numerous bones,
including a series of pre- and post-frontals, post-orbitals, and jugals

VIII. 2 PALAEONISCIDS 231

around the eyes. The outer margin of the upper jaw is covered by
premaxillae and maxillae, which are the main tooth-bearing bones.
Behind the orbital series of bones the cheek is very variable. Sometimes
there is a large bone identifiable as a pre-opercular, with a series of
opercular bones behind it. The lower portion of the throat was covered
by a series of gular plates. The spiracle in these early forms opened
above the opercular bones. The pectoral girdle was attached to the
back of the skull by a supracleithrum, below which a cleithrum and
clavicle made a series of dermal bones behind the gills, covering the
cartilaginous girdle. The roof of the mouth contained a median para-
sphenoid, with paired prevomers in front of it, and a series of
pterygoid bones occupied the space between it and the edge of the
jaws, the palatine, ectopterygoid, pterygoid, and sometimes others.
Finally the lower jaw, besides the main dentary carrying the teeth,
shows many small bones such as the pre-articular and coronoid on
the inner surface; splenial, angular, and surangular on the outside.

It will be clear that this skull of *Cheirolepis may be closely com-
pared with the skull of a crossopterygian or a modern teleostean.
The general plan is related to that of the lateral line organs arranged
along occipital, supratemporal, and infra-orbital lines. The numerous
small bones are evidently similar in the different groups, though it is
not easy to assign a suitable name to every one of the more numerous
bones of the earlier forms.

These palaeoniscids from the Middle Devonian were rather rare
freshwater fishes ; they had sharp teeth and probably lived on inverte-
brates. We have no information about their internal anatomy, but it
seems not unlikely that the air-bladder possessed a wide opening to
the pharynx (as it still does in Polypterns, descended from this stock)
and that they breathed air, as did other Devonian fishes. However,
they did not have internal nostrils, which are found in the old crosso-
pterygians.

During the Carboniferous and Permian the palaeoniscids were
numerous, mostly as small, sharp-toothed fishes. Several distinct lines
became laterally flattened and acquired an outwardly symmetrical tail
and blunt crushing teeth (Fig. 147). These characteristics probably
indicate a habit of feeding in calm waters, perhaps mainly on corals,
and they have appeared several times in the actinopterygian stock
(p. 241). Palaeoniscids of this type were formerly placed together in
a family Platysomidae, but it is now considered probable that the
type arose independently several times; thus * Amphicentrum is found
in the Carboniferous, *PIatyso?nus and *Dorypterus in the Permian,

(232)

Solea

Uranoscopus

Fig. 146. Various actinopterygians.

viii. 2 PALAEONISCIDS 233

*Cleithrulepis in the Triassic. Similar forms arose again later among
the holosteans and teleosteans and we have therefore evidence that
this type of animal organization tends to evolve into deep-bodied
creatures. *Dorypterus further resembles modern teleosteans in a great
reduction of its scales and in the forward movement of the pelvic fins.

Towards the end of the Triassic animals of typical palaeoniscid
type became rare; they were replaced by their more active and speedy,
mainly marine descendants, the Holostei (p. 234). Certain of the lines
that branched off in the Palaeozoic have, however, survived to the
present time, and in spite of subsequent specializations they give us
some idea of the characteristics of these early Actinopterygii. Perhaps
the most interesting of these survivals are Polypterus, the bichir, and
the related Calamoichthys, both inhabiting rivers in Africa. The air-
bladder shows some similarity to a lung. It forms a pair of sacs lying
ventrally below the intestine and opening to the pharynx by a median
ventral 'glottis' (Fig. 157). This is the arrangement found in lung-
fishes (except Ceratodus) and in tetrapods, and it seems reasonable to
suppose that it has survived in Polypterus from Palaeozoic times.
However, it is not certain to what extent the air-bladder is still used
as a lung, for Polypterus cannot survive out of the water.

This fish shows many other ancient characteristics. The covering
of thick rhomboidal scales, hardly overlapping, gives the animal an
archaic appearance; the structure of the scales is 'palaeoniscoid'. In
the skin there is a layer of denticles outside the scales. The presence
of a spiracle, the arrangement of the skull bones, and many other
features suggest that Polypterus is essentially a palaeoniscid surviving
to the present day. In the intestine there is a spiral valve, which
appears to have been present in the early Crossopterygii and Actino-
pterygii (as judged from fossilized 'coprolites') and occurs today not
only in the Dipnoi but also in sturgeons and, though much reduced, in
Lepisosteus and Amia. There is a single pyloric caecum in Polypterus
(the caeca are well developed in sturgeons, Lepisosteus, and Amid).
The tail of Polypterus is no longer markedly heterocercal, but shows
distinct signs of that condition. We can even find a parallel among
Carboniferous palaeoniscids for some of the special features of Poly-
pterus. The long body and dorsal fin are found in the fossil *Tarrasius,
which may have been close to the ancestry of Polypterus, though it
lacks the covering of scales. The pectoral fin in *Tarrasius, as in
Polypterus, has a peculiar lobed form, which has been compared with
the 'archipterygial' pattern (p. 269) and hence held to show that
these animals are related to the Crossoptergyii. The resemblance is,

234 BONY FISHES vm. 2-

however, only superficial and the plan of the fin is essentially actino-
pterygian. In the brain there is a thin pallium, thick corpus striatum,
and a valvula cerebelli. The pituitary is remarkable in that the hypo-
physial sac remains open to the mouth. In this and other features
(persistent pronephros) there are signs of neoteny.

3. Order 2. Acipenseroidei

The sturgeons are a rather isolated line descending from the palaeo-
niscids and characterized by reduction of bone. This was already
apparent in the Jurassic *Chondrosteus. Acipenser and other modern
sturgeons live in the sea but migrate up the river to breed. They may
reach a very large size (1,000 kg) and since a tenth of this is caviar
they are exceedingly valuable. They feed on invertebrates, which they
collect from mud stirred up from the bottom by a long snout. This is
flattened into a pear-shaped structure in Polyodon, the purely fresh-
water paddle fish of the Mississippi and in Psephurus in China. The
mouth of all sturgeons is small and the jaws weak and without teeth.
In Polyodon there is a filtering arrangement of gill-rakers in the
pharynx. The jaws of sturgeons hang free from the hyomandibular
and symplectic, and can be swung downward and forward during
feeding. The skull and skeleton is almost wholly cartilaginous and the
dermal skeleton much reduced. The tail is covered with rhomboidal
scales, but on the front of the body there are five lines of bony plates
bearing spines, with the skin in between carrying structures similar to
denticles. There is an open spiracle. The internal anatomy of the
sturgeons shows various features that have been held to show affinity
with the elasmobranchs ; for instance, besides the spiral valve there is
a conus arteriosus in the heart and a single pericardio-peritoneal canal.
However, there can be no doubt that they are descended from an
early offshoot from the actinopterygian line. They retain some fea-
tures lost by most members of the line, but resemble the Teleostei in
other characters, for instance a thin roof to the cerebral hemispheres.

The palaeoniscids and sturgeons may be grouped together in a
Superorder Chondrostci and placed with them is a third Order Sub-
holostei, probably a mixed group, including forms that resemble
palaeoniscids, but show various trends towards the holostean grade
of organization i*Ptycholepis).

4. Superorder 2. Holostei

During the later Permian period the palaeoniscids gave rise to
fishes of a different type, which replaced their ancestors almost com-

viii. 4 HOLOSTEANS 235

pletely during the Triassic and flourished greatly in the Jurassic. We
may group together the fishes of this type as Holostei but the term
is used variously by different authors and includes several lines, whose
relationships are not clear. The earliest holostean, *Acentrophorus
from the upper Permian, is much like a paleoniscid but with a small
mouth, shorter, deeper body and slightly upturned tail. This 'abbrevi-
ated heterocercal' tail was presumably made possible by the changed
swimming habits resulting from the use of the air-bladder as a hydro-
static organ. If the fish floats passively there is no need for a hetero-
cercal tail to direct the head downwards (p. 140). Similarly, the head
does not need to be flattened to produce an upward lift. The develop-
ment of the air-bladder has thus made possible the lateral flattening
and shortening of the body so characteristic of later Actinopterygii.
The body of holosteans was at first covered with thick ganoid scales,
but these became thinner in later types. The jaw suspension is
characteristic, the maxilla being freed from the pre-opercular. As a
result the lower jaw could now be protruded forwards in front of the
upper and a 'sucking' action, characteristic of teleosts was evolved,
the prey being drawn into the mouth from a distance (Gardiner,
i960). By a change in the insertion of the adductor mandibulae
muscle a more powerful jaw action then became possible. Some of the
holosteans achieved crushing teeth and replaced the dipnoans in the
early Mesozoic. There are various smaller distinctive holostean
features, such as the loss of the clavicle.

We do not know whether fishes of this type arose from a single
palaeoniscid stock; it is very likely that the change occurred several
times, and that throughout the Triassic and Jurassic there were
several lines with these holostean characteristics, evolving separately.
During the Cretaceous they became fewer, being replaced by their
teleostean descendants, but two holosteans survive today, Lepisosteus
the gar-pike (often written Lepidosteus) and Amia the bow-fin. These
are freshwater fishes, living in the American Great Lakes and other
parts of eastern North America, but the group is mainly a marine one,
having taken to the sea in the Trias at a time when other groups were
doing the same (palaeoniscids, coelacanths, elasmobranchs). The
basic cause of this movement is not known, but perhaps there was an
increase of planktonic and invertebrate life on which the fish depended.

Lepisosteus shows a rather primitive structure and must have
remained at approximately the Triassic stage. With its complete
armour of thick scales (Fig. 146) it presents all the appearance of
a primitive fish. The air-bladder opens to the pharynx and the

236 BONY FISHES vm. 4-

gar-pikes come to the surface to gulp air. On the other hand, it has
developed certain special features, especially the long jaws, with which
it catches other fishes, and the nearly symmetrical tail. Fossils similar
to the modern gar-pike are found in the Eocene.

Some of the later holosteans became deep- and short-bodied and
developed a small mouth with flat crushing teeth or a beak, for
instance, *Lepidotes (Trias to Cretaceous), and *Dapedius (Jurassic).
They probably browsed on corals, like the modern parrot fishes
(Scaridae). *Microdon and other 'pycnodonts' became laterally
flattened, like some palaeoniscids and the modern sea butterflies
(Chaetodontidae).

Another line of holostean evolution, developing from the original
stock, retained the streamlined body and from these both the modern
teleosteans and the amioids were evolved (Fig. 147). *Caturus (Trias
to Cretaceous) was covered with thick scales, but in *Pachycormns
(Cretaceous) they are thinner; these were active pelagic predators.
In Amia the scales became reduced to single bony cycloid scales, as in
Teleostei. Meanwhile other changes took place, the tail. fin becoming
externally completely symmetrical and the maxilla and other cheek
bones reduced. Amia has nearly reached the teleostean stage but
retains certain primitive features in the skeleton and the small eggs
with holoblastic cleavage.

5. Superorder 3. Teleostei

The groups so far considered have been nearly completely replaced
by the Teleostei, fishes derived from a holostean stock, which have
carried still farther the tendencies to shortening and symmetry of the
tail, reduction of the scales, and various changes in the skull, such as
reduction of the maxilla. The type apparently arose in the sea in late
Triassic times, but remained rare until the Cretaceous, by which time
several different lines of evolution had already begun *Pholidophorus
from the Trias still carried an armour of thick scales but may well
have given rise to *Leptolepis from the Jurassic and Cretaceous, which
is generally considered to be close to the ancestry of all Teleostei and
may be placed close to the order Isospondyli, many of which are
still alive. *Leptolepis was a long-bodied fish with the pelvic fins placed
far back, a skull with a full complement of bones, and a large maxilla.
The scales still show traces of the ganoin layer.

From some fish like these leptolepids have been derived the 20,000
or more species of bony fish found today. It is natural that in any
group of animals that has evolved relatively recently classification will

viii. 6 TELEOSTS 237

be difficult, because the separate twigs of the evolutionary bush will
show little difference from each other and there may be much parallel
evolution. It is only when intermediate forms have become extinct
that clear-cut major groups appear. It is therefore not easy to find
useful subdivisions of Teleostei; we may divide them among five
orders but most classifications require many more.

The first, Isospondyli, fish with soft rays, show primitive features
in the large maxilla, which forms the posterior margin of the upper
jaw, the persistence of an open duct to the air-bladder, and the
posterior position of the pelvic fins. Fishes of essentially similar type
are known as far back as the Cretaceous (* Port hens). Several familiar
fishes are of this type, including the salmon and trout (Salmo) and
herrings (Clupea). The order Ostariophysi is a large group of fresh-
water fishes, related to the Isospondyli. The anterior vertebrae are
modified to form a chain of bones, the Weberian ossicles, joining the
swim-bladder to the ear (p. 217). Here belong the carp and gold-
fish (Cyprinus), roach (Leucisciis), and cat-fishes (Silurus). The eels
(order Apodes) are rather isolated teleosts that diverged early from
the main stock and retain many primitive features. The fourth order,
the Mesichthyes, includes fishes such as the pike (Esox) and stickle-
back (G aster osteus) of structure intermediate between that of the
more primitive forms and the latest spiny-finned teleosts. The
pipe-fishes {Syngnathus) and sea-horses (Hippocampus) are probably
related to the sticklebacks. The flying-fish (Exocoetus) also belongs in
this group.

The members of the order Acanthopterygii are the most highly
developed fishes, characterized by the stiff spines at the front of the
dorsal and anal fins. The maxilla is short, the duct of the air-bladder
is closed, the body shortened, and the pelvic fins far forward. Fishes
of this type already existed in the Cretaceous (*Hoplopteryx) and the
condition may have been evolved along several different lines; the
group includes a vast array of modern types. Here belong the perches
(Perca), mullet (Mugil), wrasse (Labrus), John Dories (Zeus), blennies
(Blennius) as well as the gadid fishes such as the whiting (Gadus).
Anglers (Lophius), gurnards (Trigla), and the flat-fishes, the plaice
(Pleuronectes) and sole (Solea) and others, are further members of
this very large order.

6. Analysis of evolution of the Actinopterygii

Our knowledge of the history of the Actinopterygii is sufficiently
complete for us to be able to state more definite conclusions about the

238 BONY FISHES vm. 6

process of evolution than has been possible from consideration of the
more ancient and less perfectly known groups of fishes. First of all
we may emphasize the persistence of change. No actinopterygian
fish living in the Devonian is to be found today. Polypterns may be
regarded as a living palaeoniscid, showing features that were common
in the Carboniferous, but it has undergone many changes since that
time. Similarly the living sturgeons show the stage of organization
present in the Jurassic Chondrostei, but they also have changed much.
Lepisostens is in general structure similar to a Triassic holostean such
as *Lepidotes and Amia to a Jurassic one such as *Caturus, but both
have their own more recent specializations. It is not until we come to
the Tertiary history of fishes that types belonging to recognizable
modern genera can be found.

The Actmopterygii have therefore been changing slowly, but con-
tinuously, throughout the period of their existence. Was this change
dictated in some way by a change in their surroundings? Unfortu-
nately we cannot answer this question very clearly. The sea is a
relatively constant medium, though not as 'unchanging' as is some-
times supposed. In particular the relative extent of sea and fresh-
water changes frequently and perhaps because of such a change the
early freshwater actinopterygians took to the sea. Probably the life
in the sea is not constant over long periods. Almost certainly the
available nitrogen, phosphorus, and other essential elements change
in amount. We have reason to suspect that there was an increase in
the extent and productivity of the sea during the Triassic period. It
may be that such gradual changes in the life in the water, depending
ultimately on climate or inorganic changes, have been responsible for
the continual change of the fish population. However, it cannot be
said that we can detect evidence of any such relationship ; there is no
clear proof that the changes in the fish populations follow changes in
the environment. For the present we can only note the fact that change
occurs, even in animals living in the relatively constant sea.

Very striking is the fact that as evolution proceeds not merely does
each genus change but whole types disappear and are replaced by
others. Thus the palaeoniscid type of organization had disappeared
almost completely by the Trias and become replaced by the holostean.
A few members retained the old organization and still survive today
as Polypterus and the sturgeons. Similarly the Holostei, with their
abbreviated heterocercal tails, hardly survived into the Tertiary, but
were replaced by the Teleostei, only Lepisosteas and Amia remaining
to show the earlier organization.

(239)

240 BONY FISHES vm. 6

This replacement of one type by another appears much more
remarkable when we reflect that by a 'type', say the palaeoniscid, we
do not mean a homogeneous set of similar organisms all interbreeding.
Quite the contrary; the palaeoniscids included many separate lines,
each with its own peculiarities. When one 'type' therefore is thus
replaced by another it must mean either that some one of these many
stocks gives rise to a specially successful new population, which ousts
the old ones or that all the members of the stock are changing their
type together. It is not easy with a record such as that of the fish,
which is far from continuous, to say which of these is true in any
particular case, but we have sufficient evidence to be sure that either
of them is possible.

There is no certain example in the Actinopterygii of a single new-
type replacing all the former ones, but the origin of the Teleostei may
perhaps show a case of this sort. It is possible that the Teleostei is a
monophyletic group, arising from a single type such as *Leptolepis
and proving so successful that nearly all creatures of previous types
soon disappeared.

The Actinopterygii provide also examples of the other and perhaps
even more interesting process, the parallel evolution of a number of
different lines. There can be no doubt that from Palaeozoic times
onwards several independent lines of fishes have shown similar
changes. The tail has become shorter and more nearly symmetrical,
the body has become flattened and deepened dorso-ventrally, while
the pelvic fins have moved forward and the scaly armour has been
reduced, all of these being signs of a more effective swimming and
steering system (p. 244). As we come closer to modern times and the
geological record becomes more complete we obtain more and more
critical evidence that such changes have occurred in separate popula-
tions. Thus in the descendants of the holosteans we can recognize at
least three such lines, that leading to the round-shaped *Microdo?i,
another leading through *Caturus to Amia, and a third through
*Leptolepis to the Teleostei; probably there were many others. The
important point is that although each line possessed peculiar speciali-
zations of its own, they all showed some shortening, development of
symmetry of the tail, and thinning of the scales.

It is a considerable advance to be able to recognize such tendencies
within a group. We begin to see the possibilities of a general state-
ment on the matter. Instead of examining a heterogeneous mass of
creatures called Actinopterygii we can recognize an initial palaeoniscid
type and state that in subsequent ages this has become changed in

viii. 6 EVOLUTIONARY CHANGES 241

certain specified ways and even at a specified rate. Imperfect though
our knowledge still is, it enables us to approach towards the aim of our
study, to 'have in mind' all the fishes of actinopterygian type.

This is to make the most of our knowledge: there remains a vast
ignorance. We cannot certainly correlate this tendency of the fishes
to change with any other natural phenomena. Put in another way,
we do not know why these changes have occurred. The sea certainly
did not stay the same, but it does not seem likely that its changes have
been responsible for those in the fishes. It would be very valuable to
be able to make a more certain pronouncement on this point, for the
case is one of crucial importance. On land the conditions are con-
stantly changing, and therefore we often find reason to suspect that
changes in the animals are following environmental changes. But
can this be so in the water?

The evolutionary changes in the Actinopterygii certainly involve a
definite difference in the whole life. By development of the air-
bladder as a hydrostatic organ the animals have become able to
remain at rest at any level of the water, and thus, by suitable modifica-
tion of the shape of the body and fins, to dash about with remarkable
agility in pursuit of prey or avoidance of enemies. This has enabled
them to dispense with the heavy armour and thus further to increase
their mobility. But what made it necessary to adopt these changes?
Not surely any actual change in the sea itself. We must look then for
some factor imposed on the situation by the fishes themselves or the
neighbouring animals that constituted their biotic environment. Is
it the pressure of competition that has been responsible for the change
in fish form ? It may well be that the presence of an excess of fishes
has led them continually to search for food more and more actively,
and in new places, with the result that those types showing the greatest
ability have survived. Given the initial genetic make-up of the
palaeoniscids, further agility is most easily acquired by those fishes
in which competition tended to produce shorter tails, thinner scales,
and the other characteristics towards which the animals of this group
tend.

The fact that the same set of changes can be produced independently
from several different populations of approximately similar type
(and presumably genetic composition) is strikingly shown by the
specialized creatures evolved for life in coral reefs. Animals with
rounded bodies and small mouths, sometimes with grinding teeth,
have appeared independently several times; in the Carboniferous,
*Amphicentrnm\ Permian, *Platysomus and *I)oryptents; Triassic

242 BONY FISHES vm. 6

*Cleithrolepis\ Jurassic *Microdon and *Dapedius, and in some modern
teleosteans such as parrot fishes (Scaridae) and butterfly fishes
(Chaetodontidae). This is very valuable evidence of the way in which a
common stimulus can work on genetical constitutions that are simi-
lar but not identical. In this example the stimulus is a particular set of
environmental conditions; in other cases a similar effect may be pro-
duced by the stimulus of competition between animals, which was
probably the 'cause' of the common changes that affected so many
descendants of the palaeoniscids.

The history of these fishes therefore gives plausible ground for the
belief that the driving 'forces' that have produced evolutionary change
are the tendencies of living things to do three things: (i) to survive
and maintain themselves, (2) to grow and reproduce, (3) to vary from
their ancestors, all of these operating under the further stress of any
slow change in the environment.

Finally we must consider whether this change in the fishes can in
any way be considered to be an advance. Several times we have found
ourselves implying that this is so, that the later teleosts are 'higher'
than their Devonian ancestors. We shall be wise to suspect this judge-
ment as a glorification of the present of which we are part. However,
perhaps this danger is less marked when we are dealing with fishes not
ancestral to ourselves, whose 'advance' does not therefore bring them
nearer to man. The judgement can be put into quite specific terms:
the later Actinopterygii are 'higher' than the earlier ones because they
are more mobile, quicker, and can live free in the water with lesser
expenditure of energy than their ancestors. Unfortunately we have
no means of estimating the total amount or biomass of fish matter
that is supported by the teleostean organization, but it seems possible
that it is absolutely greater than that of any previous type, say the
holostean or palaeoniscid. If this is true, the change in plan of struc-
ture has perhaps led to an increase not only in fish biomass but in the
total biomass of all life in the sea.

The teleostean plan has certainly allowed for the development of a
great range of specializations, fitting the animals to all sorts of situa-
tions in the sea and fresh water. We must therefore not forget this
adaptability in judging the status of the group: it seems likely that
modern teleosts are more varied than any of their ancestors. This
power to enter a wide range of habitats not previously occupied is
perhaps the clearest sign of all that a group has 'advanced', and we
have already suggested that it is in this sense of suiting animals to
new modes of life that there has been a progress in evolution. It is

vm. 6 PROGRESS IN FISH EVOLUTION 243

true that the sea and fresh water have been in existence relatively
unchanged throughout the period that we are considering: in a sense
the fishes have not found a 'new' environment. But they have found
endless new ways of living in the water.

THE ADAPTIVE RADIATION OF BONY FISHES

The variety of Actinopterygii is so great that it would be impossible
to try to give a complete idea of it and the best that we can do is to
consider various functions in more detail and specify some of the ways
in which the animals have become specially modified.

1 . Swimming and locomotion

The teleosts have perfected in various ways the process of swim-
ming by the propagation of waves of contraction along the body.
The situation is different from that of elasmobranchs on account of
the presence of the air-bladder, serving to maintain the fish steadily
at any given level in the water. The stabilization of the animal during
locomotion has therefore become a wholly different problem, and the
fins are correspondingly changed. In the sharks the pectoral fins serve
to correct a continual tendency to forward pitching and by adjustment
of their position they are used to steer the animal upwards or down-
wards in the water.

With an air-bladder the fishes have become freed from the tendency
to remain at the bottom, which was prevalent in the more primitive
forms and is still so common in sharks that it has several times pro-
duced wholly bottom-living ray-like types. A fish with an air-bladder
needs only very little fin movement to maintain it at a constant depth
or to change its depth. As Harris puts it, 'the elaborate mechanism
of pectoral "aerofoils" and a lifting heterocercal tail is no longer needed
for the maintenance of a constant horizontal cruising plane. Con-
comitant with the loss of the heterocercal tail in evolution occurs a
rapid and tremendous adaptive radiation of the pectoral fin in form
and function.' A stage in this process seems to have been the use of
the paired fins to produce oscillating movements during hovering,
and this is still found in Amia and Lepisosteus, fishes that remain
relatively slow and clumsy.

Many of the lower teleosteans are relatively poor swimmers and
some of them, like so many elasmobranchs, have become bottom-
living. Thus in the catfishes there is a large anal fin, acting, like a
heterocercal tail, to give lift and negative pitch. The pectoral fins are
used to balance this tendency, very much as in sharks.

IX. I

FUNCTION OF FINS

245

In the more specialized teleosteans, however, the pectorals are
placed high up on the body and are used as brakes (Fig. 148). The
plane of the fins' expansion is vertical and they thus produce a large
drag force and a small lift force. This lift, of course, tends to make the
fish rise in the water when stopping, and there is also a pitching

Fig. 148. Use of the paired fins for braking. A. Forces produced by the fins of
Lepomis during deceleration. The pectoral and pelvic fin planes are represented by
the heavy lines. P and V, the resultant forces on the pectoral and pelvic fin respectively.
Dotted line and force P', condition during action of pectoral fins only, pelvic fins being
held in 'neutral' position. G, position of centre of gravity. B. Sun-fish stopping by
extending pectorals. Pelvic fins amputated. Although body remains horizontal, the fish
rises during the stop. c. Front view of sun-fish producing a rolling moment by the action
of one pelvic fin. // and /, horizontal and lateral forces. (From Harris,^, exp. Biol. 15.)

moment, depending on the position of the fin in relation to the centre
of gravity, usually positive. That the fish does not rise in the water, or
pitch, when it stops is apparently due to the anterior position of the
pelvic fins, so characteristic of higher Actinopterygii, which has
puzzled many morphologists. Experiments on the sun-fish (Lepomis)
have shown that after amputation of the pelvic fins the fish rises in the
water when stopping and raises its head (positive pitch). In fact the
pelvic fins are able to produce a downward moment and they tilt
the nose downwards. By alterations in their position they can be used
to control the rising or diving movements and turning one of them
outwards produces rolling (Fig. 148). It has been suggested that the

246

BONY FISHES

pelvic fins function as keels to prevent rolling, but their amputation
in Lepomis does not produce excessive rolling. Stability in the trans-
verse plane is presumably assured by the dorsal and anal fins. The

Fig. 149. Differences in form of fishes.

A, mackerel (Scomber); B, trunk-fish (Ostracion); C, sun-fish (.Mola); D, globe-fish
(Chilomycterus); E, sea-horse (Hippocampus.); f, eel (Anguilla). (From Norman.)

use of the fins for stopping was also developed in some Mesozoic
fishes, for instance, in the Triassic coelacanth, *Laugia, which pos-
sessed high pectorals, and pelvic fins in the anterior position.

In the fishes with high pectoral fins, therefore, the pelvics are
usually found far forward. In the flying-fish (Exocoetus), however
(Fig. 151), high pectoral fins are found with posterior pelvics. In this
position the pelvics would tend to help rather than hinder any

ix. i BODY FORM OF FISHES 247

tendency by the pectorals to produce a rise; the condition is exactly
that which would be expected in a flying-fish.

With these increased opportunities for delicate control of movement
without the devices of flattening of the front part of the body and a
heterocercal tail, the bony fishes have also been able to make many
other improvements in the efficiency of their swimming. The caudal
fin has, of course, adopted its symmetrical shape and is used to increase
the efficiency in turning. After its amputation a fish is not able to turn
in its own length as normally.

With shortening of the body and its lateral flattening all sorts of
new factors in streamlining the body are developed, but the details
are difficult to understand. The nature of the turbulence produced
by the movements of such a complicated structure is far from clear,
but it seems probable that the shape of the higher fishes is such
as to reduce the total skin-friction and to increase the efficiency of
swimming. Other factors such as the flexibility, which has an impor-
tant influence on the efficiency of the propulsive mechanism, have
also been changed, again in ways not fully understood, by the special
developments of the vertebral column and ribs. The speed that can
be reached increases with the length of the fish. Cruising speeds, which
are maintained for hours, are of the order of three to six times the
body-length per second, the relationship varying with the species.
During sudden bursts the speed may be much greater. Thus Bain-
bridge found that 10 L/sec could be maintained only for one second,
5 L/sec for 10 sec, and 4 L/sec for 20 sec (in dace, goldfish, and trout).

The locomotion of each type of fish is adapted to its habits. Most
freshwater fishes are 'sprinters' but there are varying degrees of
staying power. Thus we may distinguish (1) typical sprinters (pike
and perch), (2) sneakers (eel) with some staying power, (3) crawlers
(rudd, bream), with considerable staying powers for escape, (4)
stayers, either for migration (salmon) or for feeding (carp). In the fish
with staying powers there is a lateral strip of narrow red muscle fibres
in addition to the characteristic broad white fibres of fish muscles.

Bathypelagic fishes, living in deep waters, below the thermocline
at about 75 m, encounter special problems. Here currents and tur-
bulence are low, but since the water is cold it is very viscous, making
swimming difficult but sinking slow. Many deep-sea fishes have
elaborate lures, often phosphorescent. They may be described as
'floating fish traps'. They often have no swim-bladder and achieve
an almost neutral buoyancy by great reductions of the skeleton and
muscles (e.g. Ceratias). The only parts to be well ossified are the

248

BONY FISHES

IX. i-

jaws. On the other hand, deep-sea fishes that retain the swim-bladder
have a well-developed skeleton and powerful muscles (Marshall,
i960).

2. Various body forms and swimming habits in teleosts

Departures from the streamlined body form typical of pelagic fishes
have been very numerous; in nearly every case they are associated
with a reduction in the efficiency of swimming as such and the
development of some compensating protective mechanism (Fig. 149).
Lateral flattening, which is already a feature of all teleostean organiza-
tion, is carried to extremes in many types. Thus the angel-fish,

P£5tl£!!

Fig. 150. The angler-fish, Lophius.

Pterophyllum, often seen in aquaria, is provided with long filaments
and a brilliant coloration, which, in its natural habitat (rivers of
South America), give it a protective resemblance to plants, among
which it slowly moves. The flat-fishes (plaice, sole, halibut, &c.) have
carried this flattening to extreme lengths. They feed on molluscs and
other invertebrates on the sea bottom and lie always on one side.
The upper side becomes darker and protectively coloured, the lower
side white. In order to have the use of both eyes the whole head is
twisted during the post-larval period. These forms are mostly poor
swimmers, but their coloration gives them a remarkable protective
resemblance to the background (p. 257).

The John Dory (Zeus faber) has made a different use of lateral
flattening. The fish is so thin that its swimming is very slow, but
being inconspicuous when seen from in front it can approach close to
its prey, which it then catches by shooting out its jaws.

Flattening in the dorso-ventral plane is less common among teleosts
than selachians. The flattened forms are mostly angler-fishes, of

ix. 2 BODY FORM OF FISHES 249

which there are several different sorts; Lophius piscatorins (Fig. 150)
is common in British waters. It is much flattened, with a huge head
and mouth and short tail. It 'angles' by means of a dorsal fin, modified
to form a long filament with a lump at the end, which hangs over the
mouth. Swimming, though vigorous, is slow, and protection (both for
attack and defence) is obtained by sharp spines, protective coloration,
and flaps of skin down the sides of the body, which break up the
outline. There is even a special fold of pigmented skin over the lower
jaw, serving to cover the white inside of the mouth.

Other anglers are the star-gazers, Uranoscopiis of the Mediter-
ranean and Astroscopes from the Western Atlantic seaboard. Their
lure is a red process attached to the floor of the mouth and they lie in
wait buried in the sand, with the mouth opening upwards and only
the eyes showing. The colour is protective, there are poison spines,
and in Astroscopus there are electrical organs located near the most
vulnerable spot, the eyes, and formed from modified eye-muscles

(P- 253)-

Other fishes abandon the swift-moving habit for the protection
afforded by the development of heavy armour, such as that of the
trunk-fish (Ostracion) and the globe-fish (Chilomycterus) (Fig. 149).
Special spinous dorsal rays, such as those of the sword-fish {Xiphias)
may be developed, without loss of the swift-moving habit; indeed
these fish are among the fastest swimmers. There are many groups in
which an elongated body form like that of the eel has been developed.
In Anguilla itself this is associated with the habit of moving over land.
The Syngnathidae, sea-horses and pipe-fishes, no longer swim with
the typical fish motion but by passing waves along the dorsal fins.
The long and often grotesquely cut-up body form gives a strong
protective resemblance to the weeds among which they live and on
which they feed. The tail of the sea-horses has lost its caudal fin and
is used as a prehensile organ, being wrapped around the stems of
sea-weeds for attachment.

Evidently the mastery that the Actinopterygii have acquired in the
water has depended to a large extent on the freedom given by the use
of the air-bladder as a hydrostatic organ. This gives special interest to
the question of how this use first began. If we are right in supposing
that the bladder was first a respiratory diverticulum of the pharynx,
can we suppose that its value as a hydrostatic organ depended on any
exertion of effort of the fishes, or was this a case in which those born
with the organ better developed found themselves with an advantage ?
It would seem that the latter orthodox Darwinian interpretation is the

BONY FISHES

250 BUIM fiStltb IX. 2-

more likely; we can hardly imagine the fishes striving to make their
bladders bigger. But it must be remembered that only those that were
active swimmers, continually venturing into new waters, would be
able to make full use of the new organ.

Fig. 151. Various fishes showing special conditions of the pectoral fins.

A, eagle-ray (Myliobatis); B, dog-fish (Scyliorhimis); c, tunny (Thynmis) ; D, thread fin

(Polynemus) ; e, sun-fish (Lepomis); f, mud-skipper (Periophtlialmus); c, scorpion fish

(Pterois); n, cirrhitid fish (Paracirrhites); J, flying-fish (Exocoetus); K, catfish (Doras);

L, gurnard (Trigla). (From Norman.)

Many different fishes are able to jump out of the water, presumably
to escape enemies. Salmon and tarpon can jump to 8 or 9 ft above
the water. The flying-fishes have special structures to assist in such
jumps. In Exocoetus (Fig. 151) the enlarged pectoral fins serve for
gliding for distances up to 400 metres, but in the flying gurnards
(Dactylopterus) they are actually fluttered up and down, though the
flight is feeble.

Several types of fish have the pectoral fin modified to allow 'walk-
ing'. The gurnards (Trigld) move in this way over the sea bottom
(Fig. 151), and the mud-skipper (Periophtlialmus) chases about catch-

ix. 3 FEEDING HABITS 251

ing Crustacea and insects on land, using the pectoral fins as levers,
provided with special anterior and posterior muscles.

Fishes that live in situations from which they are likely to be carried
away develop suckers. Thus in the gobies, found between tide-marks,
the pelvic fins form a sucker. The cling-fishes (Lepadogaster) are another
group with the same habit. The remoras have developed a sucking-
plate from the first dorsal fin and by means of this they attach them-
selves to sharks and other large fish. In order to catch their food they
leave the transporting host, though they also feed on its ectoparasites.

3. Structure of mouth and feeding-habits of bony fishes

Although perhaps the majority of fishes are carnivorous, there are
species with all sorts of other methods of feeding. The more active
predators have strong jaws and sharp teeth, such as those of the pike
(Esox), cod (Gadus), and very many others. The teeth on the edge of
the jaw serve to bite and catch the prey, those on the walls of the
pharynx to prevent its escape if, as is often the case, it is swallowed
whole. The teeth can often be first lowered to allow entrance of the
prey and then raised to prevent its exit (e.g. in Lophius). In connexion
with this habit the walls of the oesophagus and even stomach are
often composed of striped muscle, capable of quick and powerful
contraction.

Many carnivorous fishes are very fierce. For instance, the blue fish
(Potnatomas) of the Atlantic move in shoals, cutting up every fish
they meet, making a trail of blood in the sea. The barracuda (Sphy-
raena) of tropical waters may attack man. They are said to chase
shoals of fish into shallow waters and to keep them there to serve for
food as required.

Other fishes feed on invertebrates and are then usually bottom-
feeders. Thus the plaice (Pleurojiectes) has developed chisel-like teeth
on the jaws and flattened crushing teeth in the pharynx; it feeds
largely on molluscs. The Labridae (wrasses) also have blunt teeth
and eat molluscs and crabs. The sole {Soled) has a weaker dentition
and eats mostly small Crustacea and worms. Fish such as the herring
{Chipea) that live on the minute organisms of the plankton have small
teeth and weak mouths, but are provided with a filtering system of
branched gill-rakers, making a gauze-like net, comparable with the
filtering system found in basking sharks (p. 181), paddle-fish (p. 234),
and whale-bone whales (p. 669).

Herbivorous and coral-eating fishes have crushing teeth similar to
those of the mollusc-eaters; indeed, many forms with such dentition

252 BONY FISHES ix. 3-

will take either form of food. The parrot-fishes (Scaridae) have a beak
and a grinding mill of flattened plates in the pharynx. With this they
break up the corals, rejecting the inorganic part from the anus as a
calcareous cloud. The Cyprinidae, including many of our commonest
freshwater fishes (goldfish, carp, perch, and minnow), have no teeth
on the edge of the jaw, hence the name 'leather-mouths'. There are,
however, teeth on the pharyngeal floor, biting against a horny pad
on the floor of the skull. These fishes are mainly vegetarians, but many
take mouthfuls of mud and extract nourishment from the plants and
invertebrates it contains.

4. Protective mechanisms of bony fishes

In general teleosts depend for protection against their enemies on
swift swimming, powerful jaws, good receptors, and brain. The
majority of them have thus been able to abandon the heavy armour
of their Palaeozoic ancestors. In many cases, however, subsidiary
protective mechanisms have been developed, and are especially pro-
minent in fishes that have given up the fast-swimming habit and taken
either to moving slowly among weeds or to life on the bottom. These
developments are a striking example of the way in which, following
adoption of a particular mode of life, appropriate subsidiary modifica-
tions take place, presumably by selection of those varieties of struc-
ture that are suited to the actions of the animal.

These protective devices may be classified as follows :

1. Protective armour of the surface of the body.

2. Sharp spines and poison glands.

3. Electric organs.

4. Luminous organs.

5. Coloration.

5. Scales and other surface armour

The typical cycloid teleostean scales have already been described.
They form a covering of thin overlapping bony plates, providing some
measure of protection, but not interfering with movement. The
hinder edges of the scales are sometimes provided with rows of spines,
and are then said to be ctenoid. In many fishes the scales bear
upstanding spines and possess a pulp cavity, which recalls that of
denticles. In the tropical globe-fishes (or puffers) and porcupine-
fishes (Diodon) these spines are very long and sharp and the puffers
are able to inflate themselves and cause the spines to project outwards,
a very effective protective device. In a few fishes the scales have

ix. 7 SPINES AND POISON GLANDS 253

become developed to form a bony armour even more complete than
that of the Palaeozoic fishes. Thus in the trunk- or the coffer-fishes
(Ostracion) the scales are enlarged and thickened into a rigid box,
from which only the pectoral fins and tail emerge as movable struc-
tures, the former apparently assisting the respiration, the latter the
swimming. These fishes live on the bottom of coral pools and have
a narrow beak with which they browse on the polyps.

6. Spines and poison glands

Sharp protective spines are often found in teleosts, especially on the
operculum and dorsal fins. These may be provided with modified
dermal glands that inject poison into the wound. Thus the European
weever (Trachinus) lives buried in the sand and has poison spines on
the operculum and the dorsal fins. It is suggested that the dark
colour of the fins serves as a warning. Some catfishes, scorpion fishes,
and toad-fishes also have poison spines. Spines may be effective even
if not poisonous; the stargazer, Uranoscopus, of the Mediterranean
and tropical waters has powerful spines on the operculum, which
inflict a most unpleasant wound if the animal is disturbed by hand
or foot while lying in the sand angling for its prey (p. 249). Lophius,
the angler, is also armed with dangerous spines. Several species of
catfish have large spines, sometimes serrated. In the trigger-fishes
(Balistidae and related families) of the tropics one or more of the fins
is modified to make a spine that can be raised and locked in that posi-
tion. These fishes have very brilliant coloration, but since some of
them live in the highly coloured surroundings of coral reefs it cannot
be considered certain that the colours serve as a warning.

7. Electric organs

The power to produce electric discharges has been developed
independently in four distinct families of teleosts, as well as in
torpedoes and rays. The electric organs arise bilaterally from modified
muscle fibres, the cells of which are plate-like and arranged in rows,
the electroplaques. Each plate is innervated on only one surface by
motor neurons whose activity is controlled from the forebrain, in
some fish there is a controlling nucleus located in the medulla. The
physiological properties of transmission at the nerve endings with the
electroplaques are similar to those of motor end plates. Unlike other
electrogenic tissues such as muscle or nerve, electric organs can

254 BONY FISHES ix. 7-

develop appreciable voltages in the surrounding fluid, up to 550 volts
in Electrophorus, the electric eel of the Amazon. These voltages are
achieved by series summation of the electromotive forces generated
by the individual cells.

The columnar array of several hundreds or thousands of electro-
plaques in series in the strongly electric fish, Electrophorus, Malapterurus
and Torpedo are paralleled so that the electric organs of these fish can
generate considerable current at high voltage. A maximum peak power
of up to 600 watts has been observed in T. nobiliana. The electric
organs form the major part of the body of the strongly electric fish.
The discharges are used for offence and defence. The weakly
electric fish (Gymnotidae, Mormyridae) have only a few columns
of series arrays, and relatively few electroplaques in each column.
However, many of the species emit pulses of low voltages more
or less continuously and regularly (60-400/sec). These pulses prob-
ably serve as the power components in an electrical guidance
system. All species of the continuously emitting fish are sensitive to
changes in the conductance of the water. Presumably the fish sense
the altered electric field of their discharges; although the receptors
have not yet been identified specialized lateral line organs (mormyro-
masts) are often present.

8. Luminous organs

Fishes of many different families live at great depths and 95 per
cent of individuals caught below 100 fathoms are luminescent. The
development of luminescent organs is therefore a further example of
parallel evolution. The organs usually show as rows of shining beads
of various colours on the sides and ventral surface of the fish.

In many species the light is due to organs containing luminous
bacteria, whose appearance may be controlled by the movement of a
fold of skin, or of the whole organ, or of chromatophores. Some
teleosts, however, have self-luminous photophores and these are also
found in Spinax and a few other Squalidae. They are formed from
modified mucous glands, and may be provided with reflectors and
even lenses. They can be flashed on and off, probably by sympathetic
stimulation.

The luminous organs probably often serve for recognition of the
sexes and often show distinctive patterns. They may serve to startle
attackers and in a few cases to illuminate the prey. In the deep-sea
anglers (Ceratias) the luminous tip of the fin is used as a lure.

IX. 9 (255)

9. Colours of fishes

The bony fishes show perhaps the most brilliant and varied colora-
tion of any animals, rivalling even the Lepidoptera and Cephalopoda
in this respect. The enormous range of colour and pattern provides
an excellent example of the detailed adjustment of the structure and
powers of animals to enable them to survive. A great difficulty is
introduced into the study of animal coloration by the fact that we are
usually ignorant of the capacity for visual discrimination possessed
by the animals likely to act as predators. Moreover, it is very difficult
for us to obtain this information. When we examine any two objects
we are able to say not merely that they are different but that one is
red and the other green. A person or animal that is colour-blind may
also be able to detect a difference, but yet remain unaware of any
distinction of colour; the objects appear to him only as differing in
brightness. In order to decide whether animals are able to distinguish
between light of two wavelengths we must present them with objects
of different colour but the same brightness.

We are therefore faced with the possibility that some of the colours
that appear to us so brilliant are to other animals merely differences of
tone, and animals to us conspicuous because coloured, when seen in
monochrome, may be protected. Some of the colours of fishes may
be only a means of producing a pattern of protective greys, as seen
through the eyes of an attacker. However, there is no doubt that some
fishes are able to discriminate between illuminated bodies which
though of different wavelength reflect light of equal brightness. In
the subsequent description of fish coloration we shall not be able to
consider predators further, but shall describe the colours as they
appear to the eye of a normal man.

The colour of fishes is produced by cells in the dermis, (a) the
chromatophores and (b) the reflecting cells or iridocytes (Fig. 152).
The chromatophores are branched cells containing pigment, which
may be either black (melanin) or red, orange, or yellow (carotenoids
or flavines). The iridocytes contain crystals of guanin, making them
opaque and able to reflect light so as to produce, where no chroma-
tophores are present, either a white or a silvery appearance. This
material is used in the manufacture of artificial pearls, the scales of the
cyprinoid Alburnus lucidus (the bleak) being used for the purpose.
The iridocytes may be either outside the scales, when they produce
an iridescent appearance, or inside them, giving a layer, the argenteum,
that produces a dead white or silvery colour. By a combination of the

256 BONY FISHES ix. 9

chromatophores, and of these with the iridocytes to produce inter-
ference effects, a wide range of colour is produced. Thus by mixing
yellow and black either brown or green is produced. Blue is usually
an interference colour.

The use of the colour by the fish may be classified, according to the
scheme introduced by Poulton, as cryptic or concealing, sematic or
warning patterns, and epigamic or sex coloration. Cryptic coloration

TpT Black chromabophore
^pa Yellow chroma tophore
o Iridocyte

Fig. 152. Coloration elements in the skin of the upper side of
a flounder (Platichthys). (After Norman.)

may be achieved in various ways and may be subdivided into two
main types: (1) assimilation with the background, (2) breaking up the
outline of the fish. Assimilation is common, but is often associated
with some degree of disruption of outline. The absence of all pig-
mentation in pelagic fishes, for instance the Leptocephalus larvae of
eels, is an example of assimilation. Fishes living among weeds, such
as the sea-horses and pipe-fishes, or Lophius the angler, often resemble
the weeds in colour, and in addition develop 'leaf-like' processes.
The colour of many familiar fishes, such as the green of the tench,
may be said to resemble that of the surroundings by assimilation.
When we consider the much more numerous examples of patterns
involving several colours the distinction between assimilation and dis-
ruption is more difficult to draw. Many free-swimming pelagic fishes
have the upper side dark and striped with green or blue, whereas the
under-side is white, the beautiful pattern that is seen in the mackerel
(Scombei). This gives them protection from above and below, the

IX. 9

COLOUR OF FISHES

257

striping probably making the animal less conspicuous in disturbed
water than it would be if of uniform colour. The white under-side also
serves to lessen any shadows, an important factor for animals that live
in shallow water; similar shading is used by land animals.

Fig. 153. Colour patterns of various tropical fishes.

A, Muraena {Gymnothorax); b, bat-fish (Platax); c, butterfly fish (Holacanthus); n, butterfly

fish {Cliaetodon); e, perch (Grammistes). (From Norman.)

Devices of spots and stripes are found on fishes that live against a
variegated background (Fig. 153). The beautiful red and brown mark-
ings of a trout are a good example. Flat fishes, living on sandy or
gravelly bottoms, adopt a spotted pattern, which gives them a high
degree of protection, and we shall see later that they are able to change
colour to suit the ground on which they rest. The brilliant colours
of many tropical fishes probably serve mainly to break up the outline,
though no doubt the surroundings in which they live are also brilliant.
Great variety of colours may be found on a single fish, especially in

258 BONY FISHES ix. 9-

thc trunk-fishes (Ostracioti), one species of which is described as
having a green body, yellow belly, and orange tail, while across the
body are bands of brilliant blue, edged with chocolate-brown. More-
over, the female has another colour scheme and was for long con-
sidered as a different species!

Colour differences between the sexes are frequent in fishes, the male
being usually the brighter. Thus in the little millions fish, Lebistes,
there are numerous 'races' of males with distinctive colours, but the
females are all of a single drab coloration. The genetic factors that
produce the various types of male are carried in the Y chromosome.
Presumably the colour of the males acts as an aphrodisiac as a part
of the mating display, but the significance of the different races is not
known.

Sematic or warning coloration involves the adoption of some strik-
ing pattern that does not conceal but reveals the animal. This type
of colouring is found in animals that have some special defence or
unpleasant taste (such as the sting of the wasp), and its use implies that
animals likely to attack are able to remember the pattern and the
unpleasant effects previously associated with it. It is not easy to be
certain when colours are used in this way, but it is possible that the
conspicuous spots on the electric Torpedo ocellata have this function.
Among teleosts there is the black fin of the weevers {Trachinus), pos-
sibly a warning of their poison spines, and the spiny trigger-fishes
and globe-fishes (p. 253) also have conspicuous colours.

10. Colour change in teleosts

In spite of the reputation of the chameleon the teleosts are the
vertebrates that change their colour most quickly and completely.
The melanophores are provided with nerve-fibres (Fig. 154), and
these cause contraction of the pigment and hence a paling of the skin
colour. The processes of the cells themselves are not withdrawn, the
colour change is produced by a movement of pigment within them.

The nerve-fibres in question are post-ganglionic sympathetic fibres,
leaving the ganglia in the grey rami communicantes (Fig. 139) to all
the cranial and spinal nerves. The pre-ganglionic fibres that operate
them, however, emerge only in a few segments in the middle of the
body (Fig. 235), so that severance of a few spinal roots will affect the
colour of the whole body. When a nerve to any part of the skin is cut
the chromatophores in that region at first expand, making a dark area
(Fig. 155). After a few days, however, the skin involved gradually
becomes lighter, the process, it is alleged, beginning at the edges and

IX. IO

COLOUR CHANGE

259

moving inwards. Parker, who has made a careful study of these
phenomena, believes that they indicate the presence of melanophore-
expanding nerve-fibres (said to be of 'parasympathetic' nature). Fol-
lowing the cut these fibres are supposed to be stimulated to repetitive
discharge and hence to make the dark band. Later the band pales

Fig. 154. Nerves of the melanophores of a perch. (From Ballowitz.)

Fig. 155. Diagrams showing, left, a cut in the tail of the fish Funduhis producing

a band of dark melanophores; right, when the dark band has faded a second cut

makes the melanophores again dark. (After Parker, Quart. Rev. Biol. 13.)

because the stimulating substances ('neurohumors') produced at the
nerve-endings of the melanophore-contracting fibres in the neigh-
bouring areas diffuse in gradually.

This hypothesis involves two physiological propositions which are
so novel that they would require detailed evidence for acceptance.
Firstly the act of cutting is presumed to set up a discharge of impulses
lasting for several days, which is unlikely. Moreover, the discharge is
presumed to be only in the melanophore-expanding fibres and not in
those that produce contraction. Secondly, electrical stimulation of
nerves in teleosts always produces paling and never darkening (except

2 6o BONY FISHES ix. 10-

after the use of ergotamine). We must assume, therefore, that this
form of stimulation has the opposite effect to section and only stimu-
lates the melanophore-contracting nerve-fibres. Since neither of these
propositions is adequately demonstrated, we must reject the hypo-
thesis and say that there is not sufficient evidence of melanophore-
expanding nerve-fibres.

There is, however, another agent that causes expansion of melano-
phores in a wide variety of vertebrates, namely the posterior lobe of
the pituitary(see p. 206), and there is evidence that this works also in
teleosts. Hypophysectomized specimens of the Atlantic minnow
Fiindulns are nearly always lighter than normal individuals, especially
when on a dark background. Injection of posterior pituitary extracts,
or placing of isolated scales in the extract, causes expansion of the
chromatophores of any teleost. We may conclude that colour change
is produced by the nerve-fibres tending to make the animals pale and
secretion of the posterior pituitary to make them dark. Adrenaline
induces contraction of chromatophores, and is presumably similar to
the sympathetic transmitter.

It is more difficult to decide how external influences are linked with
this internal mechanism. Fishes mostly become pale in colour on a
light background and vice versa, and the effect is produced pre-
dominantly through the eyes. There may also be a slight direct effect
of light on the chromatophores. The change in colour begins rapidly,
but its completion may take many days. Analysis of the rates of
change in normal fishes and in those with anterior and posterior
pituitary removal has led to the suggestion that the anterior lobe
produces a substance tending to make the fish lighter in colour, at
least in the eel. A similar hypothesis has been fully worked out by
Hogben and his colleagues in amphibia (p. 300). The colour is also
influenced by the pseudobranch, a secretory tissue in the first gill
arch. After removal of this a fish becomes dark and the choroid gland
of the eye, which receives blood from the pseudobranch, degener-
ates. It is suggested that the pseudobranch produces a hormone,
whose entry into the circulation is controlled by the choroid gland.

The value of the colour change in bringing the animals to the same
tint as their surroundings is considerable. Fishes kept on a light back-
ground are very conspicuous for the first few minutes when trans-
ferred to a dark one. The fisherman acknowledges this by painting
the inside of his minnow-can white, to ipake the bait conspicuous. In
the flat fishes, living on the sand, the protection assured by the colour
change is of special importance. It has been suggested that it is pos-

RESPIRATION

261

sible for the fish to assume a pattern similar to that of the ground
on which it lies, but it is probable that the degree of expansion of the
chromatophores is adjusted to suit the amount of light reflected from
the ground; by increasing or decreasing the areas of dark skin, effects
approximately appropriate to various backgrounds are produced.

Fig. 156. Special respiratory apparatus, A, in climbing perch (Anabas); b, Indian
catfish (Saccobranchus); c, African catfish (Clarias). (From Norman.)

11. Aerial respiration and the air-bladder

Many fishes are able to live outside the water. The excursions on to
the land vary from the wriggling of the eel through damp grass to the
life of the Indian climbing perch {Anabas) spent almost entirely on
land. In the eel there is no special apparatus for breathing air (though
oxygen may be taken in through the skin). The climbing perch is pro-
vided with special air chambers above the gills (Fig. 156) and even
when in water it comes to the surface to gulp air and will 'drown' if
prevented from doing so, even though it is placed in well-oxygenated
water.

Many other fishes gulp air, especially those living in shallow tropical
waters, which readily become deoxygenated. There may be other
special mechanisms for gaseous interchange. In the Indian catfish

262

BONY FISHES

IX. 11

Saccobranchns there are large air sacs growing a long way down the
body from the gill chambers (Fig. 156).

The air-bladder, which has contributed so largely to the success of
the later teleosts, may have arisen as an accessory respiratory organ,

STURGEON AND
MANY TELEOSTS

LEPIDOSTEUS
g= AND AMIA

ERYTHRINUS

CERATODUS

POLYPTERUS AND
CALAMOICHTHYS

LEPIDOSIREN AND
PROTOPTERUS

REPTILES

BIRDS

MAMMALS

Fig. 157. Air-bladder of various fishes, seen from in front and from the left side.

A, air- or swim-bladder; ad, air-duct; D, digestive tract. (From Dean, Fishes, Living &

Fossil, The Macmillan Co., after Wilder.)

used in the same way as those described above. In all the more
primitive teleosts (Isospondyli) the air-bladder preserves in the adult
its opening to the pharynx ('physostomatous'), whereas in higher
forms it becomes completely separated ('physoclistous'). Survivals of
still earlier Actinopterygii have the opening especially well developed,
though it varies from group to group (Fig. 157). Thus in the stur-
geons there is a wide opening into the dorsal side of the pharynx.
In Amia and Lepisostens the opening is also dorsal and the walls of
the sac are much folded and used for respiration. In Polypterus
the opening is ventral and the bladder has the form of a pair of lobes
below the gut. This arrangement recalls that of the tetrapod lungs and

ix. ii THE AIR-BLADDER 263

is also found in the modern lung- fishes and presumably in their
Devonian ancestors, from which we may suppose that the tetrapods
arose (p. 276). This ventral position of the air-bladder was one of the
features that for a long time led zoologists to suppose that Polypteriis

A B

Fig. 158. Diagrams illustrating the blood-supply of the air-bladder in A, Polypterus,
b, Ceratodus, c, Aviia, and d, a teleost. The blood-vessels are seen from behind, and

cut short in transverse section.
a. dorsal aorta; aad. anterior dorsal artery from the coeliac; aav. ant. ventral artery;
ab. air-bladder; aid. anterior dorsal vein to the cardinal; ba r \ 4th aortic arch (6th of the
series); d. ductus Cuvieri; ev. coeliac artery; la. left pulmonary artery; oe. oesophagus;
pr. portal vein receiving posterior vein from air-bladder; ra. rii^ht 'pulmonary' artery ; rpv.
right (branch of) 'pulmonary'' vein; rv. right vein from air-bladder; v. left 'pulmonary'
vein. (From Goodrich, Vertebrata, A. & C. Black, Ltd.)

was a member of the crossopterygian line of fishes. It is probable,
however, that the affinity is only that which persists between all
primitive members of both Actinopterygii and Crossopterygii and
is to be taken as an indication that the air-bladder was originally a
widely open respiratory sac, or perhaps pair of sacs. Once the power
to produce a pharyngeal diverticulum had been developed it is easy
to imagine that the actual position of the opening might shift either
dorsally, as in the later Actinopterygii, or ventrally, as in the tetrapods.
The blood-supply of the air-bladder should provide some indica-
tions both of its origin and function. In Polypterus and Dipnoi there
are pulmonary arteries springing from the last (sixth) branchial arch

264 BONY FISHES ix. n-

and presumably containing venous blood (Fig. 158). Blood returns
to the heart by pulmonary veins. Essentially the same arrangement
is found in Amia, but in all other Actinopterygii oxygenated blood is
supplied to the bladder from the dorsal aorta (or sometimes from the
coeliac artery). Probably, then, the original function of the air-bladder
was respiratory, and this may still be its main function not only in
Amia and Lepisosteus but also in some of the physostomatous Tele-
ostei. However, in the majority of teleosts its dorsal position, closed
duct, and arterial blood-supply show that it has some other function
and it has long been supposed that this is concerned in some way with
flotation. The air-bladder is absent from bottom-living forms, such
as flat-fishes, Lophius and Uranoscopus, though it may be present in
their pelagic larvae.

The bladder is provided with special glands by which it is filled
and the gas they secrete is mostly oxygen; only in some physosto-
matous forms is the bladder filled by gulping air. Nitrogen and carbon
dioxide are also present and the former even constitutes the main gas
in some freshwater fishes at great depths. In the more primitive forms
gas is secreted all over the surface of the bladder, but later there
develop special anterior oxygen-secreting and posterior oxygen-
absorbing regions. The former, known as the red gland, has a special
apparatus of blood-vessels, the rete mirabile, and the latter, or 'oval',
which may be developed from the closed end of the pneumatic duct,
has a special sphincter by means of which it can be closed off.

The pressure of the gases in the swim-bladder is adjusted to make
the fish neutrally buoyant, which is achieved when the bladder
occupies 7-10 per cent of the total volume in fresh-water and 5 per
cent in marine fishes. This may involve partial pressures of oxygen,
carbon dioxide, and nitrogen many times greater than those in the
blood. The mechanism by which the gases are secreted against a
diffusion gradient of several atmospheres has been much discussed.
Carbonic anhydrase is present in the gas gland and the oxyhemo-
globin of fish blood is especially sensitive to carbon dioxide, giving up
its oxygen even at high oxygen concentration.

If weights or floats are attached to a fish it maintains its position
in mid-water by swimming while gas is secreted or absorbed. The
receptors concerned are therefore not activated by the tension in the
bladder but perhaps by the movements that are necessary when the
fish is not in equilibrium. The bladder is innervated by the vagus and
sympathetic nerves and after severing the former gas secretion ceases.

The various diverticula connecting the bladder with the ear (and

IX. 12

REPRODUCTION

265

the Weberian ossicles, p. 217) may be associated with pressure recep-
tors that assist in the control of the bladder. Loaches are famous as
fish barometers, whose behaviour can be used to predict weather
changes.

12. Special reproductive mechanisms in teleosts

The teleosts show great variation in breeding habits, the eggs being
sometimes left to develop entirely by themselves, in other cases looked
after by one or both parents, while in a few species they develop

Fig. 159. Deep-sea fish Photocorynus with parasite male attached. (From Norman.)

viviparously within the mother. Hermaphrodite individuals are not
uncommon and in some species of Sparidae and Serranidae are
invariably monoecius and self-fertilizing. The method of association
of the sexes is correspondingly varied and there are numerous devices
for bringing sexes together, such as colour differences, sound produc-
tion, and the liberation of stimulating substances into the water. In
some deep-sea fishes the male is much smaller than the female, to
which it remains permanently attached (Fig. 159). Breeding is often
preceded by a migration of the fishes to suitable situations and the
association into large shoals.

The eggs may be classified as either pelagic, if they float, or demersal,
if they sink to the bottom. In the former case they are sometimes pro-
vided with an oil globule and are exceedingly numerous. Thus a
single female turbot has been calculated to contain nearly 10 million
eggs, a cod 7 million, and a ling 28 million, whereas the herring,
whose eggs sink to the bottom, probably does not lay more than

266 BONY FISHES ix. 12

50,000 eggs. The large numbers laid by the pelagic species are pre-
sumably an insurance against failure of fertilization and especially
against random elimination of the eggs and young. The greater the
care devoted to the young by the parents the smaller the number of
eggs produced (see, however, p. 283).

Demersal eggs, especially of freshwater animals, are usually laid
with some special sticky covering, by means of which they are
attached to each other and to the bottom or to stones, weeds, &c.
Thus the eggs of many cyprinids (carp, &c.) are attached to weeds.
The eggs of salmon and trout, however, though demersal, are not
sticky. From depositing eggs on weeds it is only a short step to the
building of a nest and guarding of the eggs by one or both parents.
Thus the sand goby (Gobius minutus) lays its eggs in some protected
spot, where they are guarded by the male, who aerates them by his
movements. Quite elaborate nests may be built, as by the sticklebacks
(Gasterosteus), where pairs remain together throughout the breeding-
season. A still further development is the retention of the young
within the body. In some catfishes they develop within the mouth of
either parent. In pipe-fishes and sea-horses the males are provided
with special pouches for the young.

Although external fertilization is usual, various teleosts show
internal fertilization and the young then develop within the ovary
(Zoarces, Gambnsia, Lebistes). The mechanisms by which mating and
the nutrition of the embryos are assured in these cases show some
interesting parallels with the conditions in mammals, including the
formation of placentae or nutritive material. In Lebistes the female
adopts a special position of readiness for copulation, and this has been
shown to depend partly on an internal factor in the female and partly
on a substance secreted into the water by the male. The embryos are
not attached to the wall of the ovary but develop free in the sac, feed-
ing upon an 'embryotrophic' material, apparently produced by the
discharged ovarian follicles, which become highly vascular and remain
throughout the several months of 'pregnancy'.

Rhodeus amarus, the bitterling (Cyprinidae), shows somewhat
similar conditions (Fig. 160). Association of the sexes at mating is
here made necessary by the fact that the eggs are laid within the
siphon of a swan mussel. For this purpose the cloaca of the female
develops into a tubular ovipositor. This development takes place
under the influence of a hormone produced by the ovary. Addition of
progesterone and related substances to the water containing the fish
causes growth of the ovipositor.

REPRODUCTION

267

The full growth of the ovipositor and preparation of the female for
spawning depends on the presence in the water of the male and also
of the swan mussel. Water in which males have been kept stimulates
growth of the ovipositor. When the female is ready to deposit the eggs
she adopts a vertical position in the water and the spawning male, in

&ii?9£z&*i

Fig. 160. Male and female bitterling (Rhodeits) with swan mussel
in which eggs are about to be deposited. (From Norman.)

full nuptial coloration, swims around her. An egg passes into the
oviduct and erection of the ovipositor is produced by pressure of the
urine, produced by contraction of the walls of the urinary bladder, the
exit being blocked by the egg. The extended ovipositor is thus able
to place the egg within the siphon of the mussel and the male then
immediately thereafter sheds his sperms over the opening and they
are presumably carried in by the current. The whole process shows
the elaborate interplay of internal devices and external stimuli neces-
sary for the perfection of this remarkable method of caring for the
young. Yet the various features are all developments of systems found
in other vertebrates.

LUNG-FISHES

1. Classification

Class Crossopterygii
Order i. Rhipidistia. Devonian-Recent.

Suborder i. *Osteolepidoti. Devonian-Carboniferous

*Osteolepis; *Sauripterus; *Diplopterax; *Eiisthenopteron
Suborder 2. Coelacanthini (= Actinistia). Devonian-Recent
*Coelacanthus; *Undina; Latimeria
Order 2. Dipnoi. Devonian-Recent.

*Dipterus; *Ceratodns; Neoceratodas; Protopterus; Lepidosiren

2. Crossopterygians

Although the lung-fishes and their allies are here considered last of
all the groups of fishes, because they lead on to the amphibia, it is
important to realize that in many features they stand close to the
ancestral stock of gnathostomes. It is a mistake to consider them as
'higher' animals than, say, the elasmobranchs or actinopterygians.
Only four genera belonging to this group are found at the present
time, Neoceratodus, Lepidosiren, Protopterus, the lung-fishes of Aus-
tralia, South America, and Africa respectively, and Latimeria, recently
discovered off the east coast of South Africa and the Comoro Islands
off Madagascar. These are relics of a group that can be traced back
with relatively little change to the Devonian, and there is little doubt
that at about that period the first amphibia arose from some similar
line. The characters of the modern crossopterygians are therefore of
extraordinary interest, because they show an approach to the condition
of the ancestors of all tetrapods.

3. Osteolepids

Osteolepis itself (Fig. 161), from the middle Devonian, was the
earliest and most primitive member of the group. In appearance it
shows an obvious similarity both to palaeoniscids and to early Dipnoi
and it was probably close to the line of descent from some placoderm
ancestor to both of these groups and to the amphibia. The body was
long and the tail heterocercal. A feature distinguishing all early Cros-
sopterygii from early Actinoptergyii was the presence of two dorsal

x. 1-3 OSTEOLEPIDS 269

fins in the former. The paired fins have a characteristic scaly lobed
form, from which the group derives its name, and the skeleton of the
pectoral fin contained a basal element attached to the girdle and a
branching arrangement at the tip (Fig. 180). This plan is distinctively
different from that of the rayed fin of the Actinopterygii, but could
also easily have led to the evolution of a tetrapod limb (p. 307).

The body was covered with thick, pitted rhomboidal scales, with an
appearance very similar to that of the palaeoniscid scale. These scales
have, however, a characteristic structure known as cosmoid. Each scale
(Fig. 145) may be considered as composed of an upper layer of dentine
(the cosmine), with a hard covering of shiny vitrodentine, possibly com-
parable with enamel. Below the cosmine is a 'vascular layer' consisting
of pulp cavities in which lay odontoblasts whose processes made the
dentine. This layer in turn rests on a bony layer of isopedin. The struc-
ture appears to have some relation to that of placoid scales and no
doubt the morphogenetic processes that give rise to the isolated pulp
cavities of placoid scales are similar to those that produce the cosmoid
plates. It is usual to suggest that the latter are formed of 'fused den-
ticles', but this is of course only a manner of speaking. Denticles do
not fuse, but morphogenetic processes may occur in such a way as to
produce flat plates of dentine. Indeed, it is possible that the evolution
occurred in the other direction, that is to say that the placoid scale
is a special case of the cosmoid. The condition in which a substance is
formed nearly uniformly all over the surface of the body is a more
general one than that in which such formation occurs only in isolated
areas. Indeed, the discontinuous arrangement is a very remarkable
condition, for which we have at present no explanation. The relation-
ship of the cosmoid to the ganoid scale of early Actinopterygii is not
quite clear, but the ganoid type seems to show a reduction of the
pulp cavities and development of the shiny surface-layer. The early
Dipnoi of the Devonian possessed cosmoid scales. In later osteolepids
and Dipnoi there has been a thinning of the scales, as among the
Actinopterygii, so that the later Dipnoi are covered with thin, over-
lapping, 'cycloid' scales.

The skull of osteolepids (Fig. 161) was well ossified; there was a
series of bony plates arranged according to a pattern with a general
similarity to that of palaeoniscids (p. 230) and which might well have
been ancestral to that of amphibia. There was, however, a joint across
the top of the skull between the parietal and post-parietal bones, and
an unossified gap in the base of the skull. A movable joint at this level
persists in the living coelacanth (p. 272).

270

LUNG-FISHES

x. 3-

A most important feature, common to all crossopterygians, was
that the attachment of the jaws was autostylic, that is to say, similar
to the arrangement in amphibia and remotely similar to the earliest
gnathostomes (aphetohyoids) but different from that of modern elas-

qj. pop.

Fig. 161. Skull of Osteolepis.

d. dentary; en. external nostril; esc. extrascapulars; gu. gular;/. jugal; la. lachrymal; 1-gu.
lateral gular; fngu. median gular; mx. maxilla; op. opercular; pa. parietal; pm. premaxilla;
po. postorbital; pop. preopercular; ppa. postparietal; prf. prefrontal; qj. quadratojugal;
sop. subopercular; sq. squamosal; sut. supratemporal; ta. tabular. (After Save-Soderbergh
and Westoll, Biol. Rev. 1943.)

mobranchs and actinopterygians. The teeth of osteolepids were simple
cones, not flattened plates such as are characteristic of Dipnoi, but the
teeth on the palate show a somewhat broad folded surface and each
tooth is replaced by another growing up near it, both of these being
features found in the earliest amphibia. Sections of the teeth show a
peculiar infolding of the enamel to make a labyrinthine structure,
which is not found in other fishes but is characteristic of the teeth of
the first amphibians (p. 327).

There was only one pair of nostrils on the surface of the head and
there are gaps, which are considered to be internal nostrils, at the front

x. 4 COELACANTIIS 271

end of the palate, bordered by the premaxillae, maxillae, palatines, and
prevomers. These fishes may have breathed air; they certainly also
possessed gills, covered with an operculum.

Animals of this sort seem to have been abundant in Devonian
waters and by the end of that period had diverged into several different
lines. It is interesting that the tendencies shown by these lines arc-
similar to those that we discovered in the evolution of the Actino-
pterygii. Some of the later osteolepids became shorter in body, the
tails tended to become symmetrical (diphycercal) and the scales to

Fig. 162. Coelacanth, Latimeria chalumnae, female. Length 142 cm. Caught 1954
near Anjouan. (After Grasse.)

become thinner and overlapping. *Dip!opterax and *Eiistheiiopteron
represent separate lines from the late Devonian, both showing these
characters. Probably the development of these features depends on
the use of the air-bladder as a hydrostatic organ and the associated
changes in the method of swimming.

4. Coelacanths

The osteolepids became rare in the Carboniferous and disappeared
after the early Permian, but a line descended directly from them
remained common through the Mesozoic and still survives today.
These coelacanths (Fig. 162) show certain very characteristic features,
which enabled the strange fish brought to the museum at East
London, South Africa, to be recognized immediately as belonging to
the group. They are rather deep-bodied animals, with a characteristic
three-lobed diphycercal tail. The type first appeared in the late
Devonian and was obviously derived from osteolepid ancestry having
two dorsal fins, diphycercal tail, lobed fins, and a rhipidistian pattern
of skull bones, including in most forms a fronto-parietal joint. There
was a calcified air-bladder. *CoelacantJius and other Carboniferous

272 LUNG-FISHES x. 4-

forms lived in fresh water, but *Undina and other Jurassic and Creta-
ceous types lived in the sea.

The first living specimen of the group was fished off the east coast
of South Africa and eleven others have since been caught around the
Comoro Islands (Madagascar) (Fig. 162). All are referred to the genus
Latimeria. They have been caught near the bottom at considerable
depths (150-400 m). Unlike most of their fossil ancestors they are
large fishes, weighing up to 80 kg; they are dull blue in colour. The
whole body is covered with heavy cosmoid scales.

The notochord is a massive unconstricted rod. The skull possesses
a well-marked joint between a condyle on the hind end of the basi-
sphenoid and a glenoid cavity on the front of the base of the oto-
occipital region. This joint, together with fibrous unions between
other bones allows of movement of the front part of the head on the
hind. A large pair of muscles runs from the parasphenoid up and
back to the pro-otic and serves to raise the front part of the head on
the hind. Coraco-mandibular muscles attached to the palato-quadrate
have the reverse action and the movement is presumably concerned
with catching the prey. There are numerous small teeth on the jaws
and palate. Latimeria lives on other fishes, apparently swallowed whole
by the powerful oesophagus. There is a well-developed spiral intes-
tine.

The 'air-bladder' arises by a ventral opening from the oesophagus
and proceeds backwards and dorsally for the whole length of the
abdominal cavity. The lumen is very small and the organ is 95 per
cent fat. It may serve to reduce the specific gravity. Respiration is by
the gills. The heart shows a linear 'embryonic' condition, with the
sinus venosus and auricle behind the ventricle. There are four rows of
valves in the conus. The red cells are large, as in elasmobranchs,
Dipnoi, and Amphibia. Nothing is known of the development,
except that the eggs are large.

The brain lies far back in the cranium, of which it occupies less
than one-hundredth part, the rest being filled with fat. Its structure
is somewhat like that of a teleostean, with a thin fore-brain roof, and
large striatum, but without eversion. There is no valvula to the cere-
bellum. The pituitary cleft is large and the gland remains in continuity
with the roof of the mouth.

There are anterior and posterior nares but both open on the surface
of the head and they have nothing to do with respiration. The rostral
organ is a large median sac opening to the surface by three pairs of
canals and richly innervated by the superficial ophthalmic nerve.

x. 5 FOSSIL DIPNOI 273

A similar sac occurs in fossil coelacanths back to the Devonian but its
function is quite unknown. The eye, inner-ear, and lateral line system
are well developed.

It is hard to see what features have enabled Latimeria to survive
with little change since the Jurassic or earlier (see p. 771). It clearly
cannot be by special development of the brain or receptors. Its
habitat is isolated, but not especially protected and its population
seems to be small since even by exceptional efforts so few specimens
have been found. Perhaps they are more numerous in deeper waters.
In some of its features it shows developments parallel to those of the
Teleostei rather than to the Dipnoi, whose remote ancestry it shares.
Several of its characteristics are paedomorphic. These can hardly be
alone responsible for such a long survival, but some of them also
appear in the other survivors from the Paleozoic, Polypterus, stur-
geons, and Dipnoi.

5. Fossil Dipnoi

The Devonian Dipnoi were more like their osteolepid relatives than
are the surviving modern forms (Fig. 163). The early members of this
group, such as *Dipterns (Fig. 211), showed the typical elongated
body, thick cosmoid scales, heterocercal tail, lobed fins, and well-
ossified skull. The pattern of the bones was obscured by a seasonal
deposit of cosmine, this being periodically absorbed to allow of growth.

The individual bones have a certain similarity to those of osteolepids,
but there are extra bones that are difficult to name. There was no
premaxilla or maxilla, nor any teeth along the edge of the jaw; instead
broad, ridged tooth-plates were developed on the palate and inside
of the lower jaw, presumably as an adaptation for eating molluscs
and other invertebrates. These crushing-plates are characteristic of
the Dipnoi and preclude even the earliest of them from being the
actual ancestors of the amphibia. By the end of the Devonian the
Dipnoi were showing changes similar to those of the osteolepids and
palaeoniscids. The body became shorter, the first dorsal fin dis-
appeared, the tail became diphycercal, and the scales lost their shiny
surface-layer and became thin. The teeth of *Ceratodus appear in the
Triassic and were known to geologists long before the related living
animal was discovered. There has been very little change in this
animal in more than 150 million years, though the recent members are
placed in a distinct genus Neoceratodns.

The evolution of Dipnoi is especially interesting because the rate
of change has actually been measured (Westoll, 1949). Twenty-six

(274)

&£? ->'■#?£'?

Fig. 163. The three living lung-fishes and their distribution.
A, Protopterus; b, Lepidosiren; c, Neoceratodns. (From Norman.)

^r •

£ 40

^30

j 1

1 1 L

1 '

350

250

150

Age / Millions of years)

Fig. 164. Rate of evolution in lung-fishes. Each point represents the index of a single
genus obtained by taking twenty-six characters and rating them with grades of struc-
ture. The lowest value was given for the most primitive condition, the highest for the
most modern one. (After Westoll and Simpson.)

x. 5~6

MODERN LUNG-FISHES

275

different characteristics such as proportion of skull, nature of dermal
bones or dentition were divided into 3-8 grades. Each fossil genus
was thus given a score, the minimum being for characters appearing
in the oldest lung-fish, the hypothetical ancestor being o. Actual
scores ranged from 4 for the earliest to 100 for two of the living genera.
Plotting against time we see that there was an early acceleration of
evolution followed by very slow or zero change in the last 150 million
years (Fig. 164). It has also

been shown that a similar
method applied to the evolu-
tion of coelacanths gives a
curve of similar shape (Schaef-
fer, 1952).

6. Modern lung-fishes

The three surviving genera
of lung-fishes (Fig. 163) are
mainly inhabitants of rivers
(though Protopterm lives in
large lakes) and they all
breathe air. Neoceratodas lives
only in the Burnett and Mary

rivers in Queensland, the pools of which become very low and stagnant
in summer. Lepidosiren from the rivers of tropical South America, and
Protopterus from tropical Africa, can survive when the rivers dry up
completely. They dig into the mud, leaving a small opening for breath-
ing, and can remain in this state for at least six months. Remains of
cylindrical burrows found associated with dipnoan bones show that
this habit of aestivation has been adopted by the group at least since
Permian times. The three survivors all show similar deviations from
the conditions found in *Dipterus, but Neoceratodus has diverged less
than the other two. The tail fin is symmetrical (diphycercal) in all
three, with no trace of separate dorsal fins. The paired fins are of
'archipterygial' type in Neoceratodus, with an axis and two rows of
radials (Fig. 165). The scapula is covered by clavicles, cleithra, and
post-temporals, the latter articulating with the skull. The scales are
reduced to bony plates.

The vertebrae are cartilaginous arches, the notochord remaining
as an unconstricted rod. In the skull there is also a great reduction of
ossification, the dorsal bones consisting of a few bony plates, forming
a pattern not obviously comparable with that of other forms (Fig.

Fig. 165. Neoceratodus, showing the method of
walking on the bottom. A, forwards; B, back-
wards; C, resting. (From Ihle, after Dean.)

276

LUNG-FISHES

x. 6

166). The jaw-suspension is autostylic. The food consists of small
invertebrates and decaying vegetable matter, which is eaten in large
amounts. In the gut there is no stomach and the intestine is ciliated.
There are no hepatic caeca, but a well-developed spiral valve is
present.

PP- qc. Pa

Fig. 166. Skull of Neoceratodus. Above, Lateral view; below, view of medial surface

of right half.
a. angular; bh. basihyal; br. fifth branchial arch; ch. ceratohyal; cr. 'cranial' rib; d. dentary;
eo. 'exoccipital'; hm. hyomandibula; hn. hyomandibular nerve; hr. hypohyal; Ip. lateral
plate; ma. median anterior, and mp. median posterior plate; na. neural arch; nac. cartilage
of neural arch; ns. notochordal sheath; nsp. neural spine; nt. notochord; o. opercular, and
oc. its cartilage; pa. parasphenoid; />/. post-frontal; pp. pterygopalatine; pt. palatine tooth;
pto. pterotic (?), and g. its downward process covering the quadrate cartilage, qc; s. sub-
opercular; so. suborbital; sp. splenial; st. splenial tooth; vt. vomerine tooth. (From

Goodrich.)

The external nostrils lie just at the edge of the mouth and the
internal nostrils open into its roof. The air-bladder is developed into
a definitely lung-like structure (there is one in Neoceratodus, a pair in
each of the others), divided into many chambers. Neoceratodus has
been observed to come to the surface to breathe air and is said to be
able to survive in foul water that kills other fishes, but it cannot live
out of the water. Lepidosiren and Protopterus have been shown to
obtain 98 per cent of their oxygen from the air. The wall of the air-
bladder of all forms contains muscle-fibres and the cavity is subdivided
into a number of pouches or alveoli (Fig. 157). In Protopterus and
Lepidosiren the edges of the slit-like glottis are controlled by muscles
and there is an epiglottis. The lung is supplied with blood from the
last branchial arch in Neoceratodus (Fig. 167), but in the other Dipnoi

x. 6

CIRCULATION

277

there is a more elaborate arrangement. The second and third gill-
arches bear no lamellae and their afferent and efferent branchial vessels
are directly continuous, so that blood flows from the ventral to the
dorsal aorta and carotids. The pulmonary artery springs from the
dorsal aorta. Blood returns in a special pulmonary vein to the partly

Fig. 167. Branchial circulation of A Neoceratodus and b Protopterus.

abr. anterior efferent vessel; ac. anterior carotid, a/ 3 " 6 , four afferent vessels (corresponding
to the original arches 4-6) ; ah. afferent hyoidean ; c. conus ; cl. coeliac artery ; da. dorsal aorta ;
dl. dorso-lateral aorta; eb-~*. second and fourth epibranchial arteries; eg. external gills;
eh. efferent hyoidean; ht. heart; hyp. median hypobranchial; L. air-bladder; la. lingual
artery; mes. mesenteric artery; pa. pulmonary artery; pc. posterior carotid; pv. pulmonary
vein; 5. position of closed spiracle; va. ventral artery; vx. vena cava inferior; I-V five
branchial slits.

The gills are represented on the hyoid and next four branchial arches. (From Goodrich.)

separated left side of the sinus venosus. The auricle is partly divided
into two and the ventricle is almost completely divided by a ridge
and a series of muscular trabeculae. The ventral aorta is shortened
into a spirally twisted truncus arteriosus, provided with a system of
valves such that the blood from the left side of the auricle is directed
mostly into the first two branchial arches, that from the right side
into the last two. In this way some separation of pulmonary and
systemic circulations is achieved. Indeed, although there is every
reason to believe that the mechanism has been in existence for nearly
300 million years, it shows us most clearly a possible intermediate
stage between aquatic and pulmonary respiration. It seems likely that
the earliest amphibia employed a similar system. There is a coronary
artery arising from the anterior efferent branchial arches (Fig. 167).

278

LUNG-FISHES

x, 6

A further amphibian feature of the blood-vascular system is the

presence of an inferior vena cava, a
vessel collecting blood from the kidneys
and reaching to the heart by passing
round to the right of the gut in the
mesentery. The more dorsal cardinal
veins, joining the ductus Cuvieri, remain
present, however, and there is a renal
portal system.

The adrenals of Dipnoi are represented
by two separate masses of tissue. The
perirenal tissue of Protopterus is a con-
siderable mass of material around the
kidney, containing lipid, steroid, and
round-cell (lymphoid) tissues, as well
as endothelial and pigment cells. The
steroid tissue shows histochemical pro-
perties similar to those of mammalian
adrenal cortex and undergoes changes
after injection of mammalian ACTH.
This tissue thus shows a collection of
functions, haematopoietic, phagocytic,
storage, endocrine, and pigmentary,
which may show the starting point of
the evolution of the tetrapod adrenal
cortex. Cells that give the chrome
reaction, the adrenal medullary tissue, lie
in the walls of the intercostal branches
of the dorsal aorta. This condition could
have given rise to that of amphibia.

The arrangement of the urinogenital
system is similar to that of amphibia and
is probably closer to that of the ancestral
gnathostome than in any living elasmo-
branch or actinopterygian. In the male
there are vasa efFerentia by which sperms
are passed through the excretory portion
of the mesonephros. In the female eggs
are shed free into the coelom and carried
out by a Mullerian duct, whose opening lies far forward. An in-
teresting feature is that the Mullerian duct is very well developed in

— 1

Fig. 168. Dorsal view of the brain
of Protopterus.

I, spinal cord; 2, dorsal root of first
spinal nerve; 3, diverticula of 4, the
saccus endolyinphaticus; 5, medulla
oblongata; 6, fourth ventricle; 7,
cerebellum; 8, mesencephalon (fused
optic lobes); 9, stalk of pineal body;
10, thalamencephalon; 11, velum
transversum; 12, pineal body; 13,
lobushippocampi; i4,choroidplexus ;
15, cerebral hemisphere; 16, olfac-
tory lobe. (After Burckhardt, from
Goodrich.)

x. 6 EVOLUTION OF DIPNOI 279

the male. This is one of several details (lack of ossification, un-
constricted notochord) which raise the suspicion that the living
Dipnoi have acquired their special characters by a process of
paedomorphosis or partial neoteny, that is to say, becoming sexually
mature in an early stage of morphogenesis.

The development, again, shows similarity to that of amphibia and
dissimilarity from the other groups of fishes in that cleavage is total
and gastrulation takes place to form a yolk plug. There is therefore
no blastoderm or extra-embryonic yolk sac. However, the cells of the
vegetative pole contribute little to the shape of the embryo and indeed
may form a partially separate yolk sac. The larvae show distinct simi-
larity to those of amphibia, especially the larvae of Lepidosiren and
Protopterus, in which there is a sucker and external gills.

The nervous system shows the same affinities as the rest of the
organization (Fig. 1 68). The forebrain is evaginated into a well-marked
pair of cerebral hemispheres. The roof of these, though not very
thick, is nervous and therefore is definitely of the inverted type, not
everted as in Actinopterygii. The optic lobes are little developed, the
mesencephalon being hardlv wider than the diencephalon. The cere-
bellum is small. A peculiar feature is the development of the inner ear
to form a special lobed saccus endolymphaticus, lying above the
medulla oblongata. The significance of this is not known, but it is
interesting that similar backward extensions of the ear are found in
amphibia.

In many features, then, the Dipnoi differ from modern fishes and
resemble the amphibia, which evolved from the same stock. The early
crossopterygians probably competed somewhat precariously with
other fishes, as do the Dipnoi, and indeed many urodeles, today. It
was only after tens of millions of years of evolution during the Car-
boniferous and Permian times that numerous land animals arose,
in the form of the later amphibian and reptilian types (Fig. 211).

FISHES AND MAN

Man's influence, which has so altered the face of the land, also reaches
out into the water. During the last half-million years or so fishing has
grown continually, until at the present time in fresh and shallow sea
waters man has become the most important source of mortality of fish.
However, he still leaves vast regions of the sea, as of the land, almost
untouched. It may be that methods of catching the fish that swim
above deep waters will eventually produce changes there too, pro-
viding a substantial extension of the food-supplies of man and
effecting great alteration in the population of the sea.

Man has caught fish from his earliest times and he uses many parts
of their bodies. The skin, especially of elasmobranchs, makes a useful
leather and also a polishing material. The scales of the bleak (Alburnus)
yield a substance that when coated on to the inside of glass beads
makes artificial pearls. The lining of the air-bladder, especially of
sturgeons, makes isinglass, a shiny powder used for various purposes
as an adsorbent (i.e. in wine-making). Fish-glue is obtained from the
connective tissue of the skin and other parts. Fish oils are used as
food, and are also valuable in the manufacture of soap and other things.
Besides their direct use as human food, fish products may be fed to
animals, and the liver makes excellent manure.

Fish therefore provide the raw material for many human activities,
but it is, of course, principally for food that they are caught. From a
fish diet one can obtain not only abundant calorific value, especially
if the fish be fat, but also various proteins, often the fat-soluble
vitamins A and D, and usually considerable amounts of combined
phosphorus and other elements. Herring and mackerel are probably
the cheapest source of protein available to many people in Britain.
Fish are undoubtedly good food, and what is perhaps even more
important they are esteemed as such; most people think that they
taste good.

It is not possible to give an accurate estimate of the amount of fish
caught every year; 20 million tons, of value £200 million, is certainly
not an overestimate for the catch of the whole world in each of the
years between the Great Wars. An appreciable fraction of the nutri-
ment of the human race is derived from fish. The annual catch was
estimated at 26 million metric tons in 1951 . The greatest national

xi METHODS OF FISHING 281

catch was by Japan (3-8 million), followed by U.S.S.R. (2-5), U.S.A.
(2-3), and Great Britain (i-i).

By far the greater part of all fishing is in the sea. In Great Britain
the total catch in fresh water annually is reckoned at only 2,000 tons
and the entire stock at 8,000 tons. However, there are important
fishing industries in the American Great Lakes, the African lakes, and
in many parts of the world carp are raised on fish farms, the water
being manured to yield a good crop of the freshwater plants and
invertebrates on which the carp feed. The milk fish (Chanos chanos),
which feeds directly on algae, provides high yields in many tropical
and subtropical fish-ponds.

Fishing in the sea is limited mainly by two considerations. First,
the labour is only really profitable when the fish population is dense.
Secondly, fish do not keep well unless they are treated in some special
way and they are therefore best caught near to their market. For these
reasons the big commercial fisheries are mostly in the relatively shal-
low waters of the continental shelf (down to 200 fathoms) and in the
northern hemisphere. However, by packing the fish in ice or cooling
by other means, the vessels are now able to go longer distances than
formerly. Japanese and American vessels now fish for tuna and salmon
in the open ocean.

For catching purposes fish may be divided into those that swim
away from the bottom, the pelagic forms, such as herring or mackerel,
and the bottom-living or demersal fishes, such as the skates and rays,
flat-fishes and angler-fishes. For the first the gear employed is usually
drift-net. This is of narrow mesh and is shot and left overnight, drifting
vertically near the surface, often making a barrier two or three miles
in length. The fish, such as herrings, swim into them, and become
enmeshed, and are removed as the nets are hauled in.

The success of such fishing with drift-nets depends on laying the
nets in the path of large shoals of fish and it is therefore practised
especially in regions where fish congregate seasonally. For instance,
in the North Sea between East Anglia and Holland the herring con-
gregate in the autumn; at certain times, for unknown reasons, all the
fish in the area begin to move, making 'the swim', and they are then
caught in great numbers. Herring are usually caught at slack water.
At the October full moon, slack water occurs just after dusk and just
before dawn and catches are higher then. Other drift-net fisheries
depend on intercepting the fish when rising to feed. Evidently these
methods demand a close knowledge of the habits and migrations of
the fish. The fishermen have learned to know when and where to

282 FISHES AND MAN xi

expect the larger and nearer aggregations, but there is still much to
be done in tracing the migration and behaviour of pelagic fishes.
It is not impossible that other pelagic fisheries could be developed
that would be at least as advantageous as the herring fishery. Besides
those eaten fresh, others are preserved as kippers by salting and smok-
ing, or are heavily salted and smoked to make 'red herrings' for which
there has been a large export market.

Lining is a method that can be used for either pelagic or demersal
fish. For instance, the cod fishery of Newfoundland uses lines with
several thousand baited hooks. Inshore fishing may be accomplished
by beach seining, a process of enclosure of the fish from the shore.
There are also various forms of trap into which the fish swim and
cannot escape. Danish seining, or purse seining, completely surrounding
the fish and sometimes then also drawing the bottom of the net
together, is another effective method.

The greatest quantities of fish are caught, however, by the various
forms of trawling. These depend essentially on dragging a bag along
the bottom of the sea, and the different types adopt various means of
keeping the bag open. The earlier way of doing this was by means of
a rigid bar and these beam trawls sometimes used poles over 50 ft
long. More recently otter-trawling has replaced the beam trawl, the
otter boards being flat wooden structures attached at each end, so as
to sheer away when they are dragged through the water, thus opening
the net. Various devices are used to stir up the fish from the bottom;
in particular the otter boards are now usually separated from the net
by long wires and a 'tickler' chain is attached in front of the mouth.

With such methods very large amounts of fish can be taken from
the sea bottom. In i860 sailing-ships landed 500 tons of fish at
Grimsby; by 190 1, 176,000 tons were landed from the steam traw lers
50,000 tons of plaice alone are taken annually from the North Sea.
There is evidence that the taking of such amounts of fish from rela-
tively confined waters has a large influence on the population. For
instance, it is estimated that 45 per cent of the stock of plaice is
caught each year in the North Sea. Under these conditions man pro-
vides the main source of mortality for the fishes. It is less clear
exactly how such mortality influences the total population of the fish
in the area. There is reliable evidence that intensive fishing reduces
the productivity of fishing effort in some cases, but there is also
evidence that by reducing competition fishing may produce faster
growth of the fish. The problem is worth some further discussion
since, besides its economic importance, it gives us an insight into the

xi NUMBER OF FISHES 283

life of the vast populations of the sea and a glimpse of the factors that
control the numbers of each animal species.

It used to be held that one of the chief dangers of fishing was that
it would destroy the breeding-stock, on the grounds that it is axio-
matic that something is wrong if fish are destroyed before they have
an opportunity to breed. We may detect something of anthropocentric
sentimentality here, for reflection shows at once that it is impossible
for every fish that is hatched to survive and, further, that the total
annual supply of fish can be provided by relatively few adults. The
number of fish in the sea, indeed, bears no obvious relation to the
number of eggs. A cod may shed as many as 8 million eggs (usually
fewer), which float at the sea surface and hatch into planktonic young.
Yet herrings, which are much more numerous as adults, lay fewer
eggs, usually less than 30,000 each. Presumably the risks of life are
less for the herring, but we cannot see clearly why; the herring's eggs
are sticky and become attached to gravel or seaweeds, which may give
them some protection; they are known to be eaten by other fishes,
perhaps on a smaller scale than planktonic eggs. Both herring and
cod fry are planktonic and feed on the nauplius and other larval
stages of Calamis and other copepods. The cod, like other bottom-
fishes, has to undergo the risks of metamorphosis, but this hardly
seems sufficient to explain the much greater abundance of herring,
especially since many fishes feed on the latter, including the cod them-
selves! As Graham puts it, 'no one really knows why the herring,
which nearly everything eats, should be able to manage with a less
rate of reproduction than the cod, which eats nearly everything'.
The greater part of the mortality of pelagic fish larvae is due to pre-
dation, including that by members of the same species. This probably
provides a method of regulation, the number of each species eaten
being dependent on their frequency.

This brings us to face the difficult question of the pressure, force,
or potential that ensures and controls the number of animals. Re-
production is only a part of the source of this pressure, the other
element being the feeding and growth of the animals as a result of the
skill and persistence with which they seek and consume their food.
It is somewhat easier to study these questions in a marine than in a
land community, the whole population being enclosed in one vast
bath, the additions and subtractions to which can be known.

We must not forget, however, that conditions are far from con-
stant, even in the 'unchanging sea'. For instance, the extent to which
fish-fry hatch and successfully overcome the hazards of the early

(28 4 )

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

Ifllll

1907

■ ■*■

1908

1909

1910

1911

1912

1913

1914

M^^—

1915

1916

JLL

1917

1918

II - .1 1919

: 20

40
20

: 60

60
40
20

60 ^
40 £

60 <*
40 ^

Z0 3

-40 ^

: 20

-120

: 20

■20

Fig. i

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
Age of fish -years

69. Age composition of Norwegian herring catches 1907-19, showing
the preponderance of particular year-classes. (After Hjort.)

xi FISH CYCLES 285

stages of life varies most mysteriously from year to year. By study of
the markings on the scales, bones, and otoliths it is possible to show
the age composition of a fish population and it is found that the
hatches of certain years predominate. Thus the herring hatched in
1904 dominated the population in some parts of the North Sea for
years afterwards (Fig. 169). Subsequent good herring years occurred
in 1913 and 1918. Similarly there were good cod years in 1904 and
191 2. Haddock broods in the North Sea follow a rather regular

r <

1919

12-2

10-0

8-1

8-8

4-8*

3-8

2-3'

2-6

0-8*

(0-2

Vo 2

12J

09 s

1920 1921 1922 1923 1924 1925 1926 1927 1928 1929 1930 1931 1932 1933 1934

Year class

Fig. 170. Relative strengths of haddock broods in the North Sea, showing cyclical
fluctuations. (After Raitt, from Russell, The Overfishing Problem.)

rhythm with a period of about three years (Fig. 170). These cyclical
changes in hatching do not appear to produce fluctuations in the total
population of that species, though we have inadequate data on the
point. It seems likely that there is a limit set to the total of fish of the
species, irrespective of age-grouping.

In addition to such cyclical changes there are also larger ones, such
as the increase of cod in the far north around Bear Island in recent
years, apparently due to a northerly extension of warm water, the
reason for which is not known. Since so many changes are going on
in the eternal sea is it to be wondered at that the animals in it are
changing? We might be surprised rather at the slowness of their
evolution.

All the fish-life in the sea depends ultimately on the diatoms,
flagellates, and other green organisms of the plankton, reaching the
fish usually after passage through one or more animals, especially
copepods. Bottom-living fishes also depend on plankton, in this case

286 FISHES AND MAN xi

after it has died and passed through a bottom-living invertebrate.
Thus plaice feed on lamellibranchs and worms, soles on worms alone,
haddock on star-fish, molluscs, and worms. The phytoplankton is,
of course, built up by photosynthesis from carbon dioxide, water,
nitrates, phosphates, and small quantities of other substances. The
limiting factors in the plankton growth, granted adequate temperature
and sunlight, may be nitrate, ammonia, and phosphate, the latter
present only to the extent of less than one part in 20 million. During
the spring and early summer nearly all the phosphate in the water may
be taken up into the phytoplankton, which increases rapidly. The
zooplankton (Cala?ius, Sec.) increases somewhat later and by mid-
summer grazes down the phytoplankton to a considerable extent. It
is at this midsummer period that the pelagic fishes feed most easily,
and a little later it is the turn of the bottom-living invertebrates and
fish, as some of the zooplankton dies and falls to the bottom. At the
end of the season there may be a second increase in the phytoplankton,
the recovery being due to breakdown of the discontinuity layer (see
below), and then with the onset of winter the plants die off and most
of the phosphate is returned to the inorganic condition.

Thus to take the case of the cod, whose food chain is one of the
longest: the activity of the plants turns carbon dioxide, nitrate, and
phosphate into organic matter: the activity of the copepods makes
this available to the herrings and the cod eat the herrings. There are,
of course, many intermediate effects: Sagitta eat some of the cope-
pods, fish-fry and large cod eat younger cod, and so on, but in general
we shall not go wrong if we assume that the cycle depends on the
activity of diatoms, calanoids, herrings, and codfish— all seeking,
eating, growing, reproducing, and dying.

The pressure of these various activities produces a complicated set
of interrelations that may without undue extravagance of fancy be
called a macro-organism. The activities of all the members contribute
to the balance that is set up. Sometimes shortage of materials, such as
phosphorus, at key-points may determine the whole cycle.

The phosphate in the sea is increased to a small extent by drainage
from the land and, further, in a restricted area such as the North Sea,
by the influx of water from more open areas, in that case the Atlantic.
Not all the phosphate in a given area of sea is available for organic
growth, because there is usually a separation between upper and lower
layers owing to the upper layer becoming warmer and less dense. The
phosphate in the water below this limiting discontinuity layer, usually
lying 20-100 metres down, is thus not available, though it may be

xi SIZES OF FISH CAUGHT 287

made available in certain areas by particular conditions that lead to
up-currents and mixing of the layers.

With these facts in mind we can now make further inquiry into the
effects on the population of the sea of removal by man of large quanti-
ties of organic matter in the shape of fish. There are enough data to
give us hints of the changes that follow, and the hope that with further
study we may eventually understand the Great Sea Beast sufficiently
well to be able, if we can control ourselves, to regulate its growth to
our advantage.

In a few cases it has been possible to follow the course of a fishery
from its early beginnings, with few vessels and simple apparatus,
through stages in which the fishing was progressively more intense.
The statistics are seldom adequate to provide us with wholly satis-
factory conclusions, but they suggest that (1) as fishing becomes more
intense, the yield per unit of fishing power declines ; that is to say, the
industry becomes relatively less profitable; (2) in spite of this, the
total yield may remain constant, or somewhat increase, even though
(3) the average size of the fish caught decreases.

For example, fishing for plaice in the Barents Sea, north of Nor-
way, was begun in 1905, and the almost 'virgin' population in 1907
showed great preponderance of large mature fish; whereas in the
North Sea, which had already been fished for many years, the average
size was much smaller and few of the plaice were mature. The fish
taken in the Barents Sea were old and had grown slowly. Transplanta-
tion of fish of this stock to the North Sea, however, proved that they
were able to grow as rapidly as the local fish. Some measure of the
intensity of fishing is given by the number of days' absence of vessels
fishing in a given area. No doubt the measure is inexact, particularly
if the methods used are changed, but it provides the best estimate
available. The landing of plaice taken from the Barents Sea per day's
absence was 347 cwt in 1906, 50-4 cwt in 1909, and then fell to 46-3,
33-7, and 20-5 cwt in the following years. The total yield showed some
decline. The sequence of events is typical of what happens when a
stock of mature fish is first exploited.

Graham described a good example of a similar situation in Lake
Victoria-Nyanza, where he found two stocks of the carp-like fish
Tilapia, one fished heavily and the other with primitive devices only.
The less heavily fished stock contained five times as many fish as the
other and they were much older. Yet by the intensive fishing the
poorer stock was being made to yield a ten times greater weight than
the richer stock. This desirable state of affairs for man in general is

288 FISHES AND MAN xi

considered unsatisfactory by the fishermen, since the yield per unit of
effort is much greater when the richer stock is fished.

The yield of haddock in the North Sea per day's absence averaged
5 -8 cwt between 1906 and 191 3, rose to 15-8 cvvt in 19 19, averaged
6-5 cvvt in 1 922-1 929, and 3-7 cwt in 1930-7. The fish are divided into
large, medium, and small categories, and the percentage of the last
category was 50 before the war, 70 in 1922-9, and 85 in 1930-7;
evidently the fish were becoming smaller throughout this period, yet
the total haddock catch changed only slightly, from 121 million kg
( 1 910-13) to 138 million kg (1922-9) and 94 million kg (1930-6).
Fishing seems to have made the population consist of smaller fish,
giving a smaller yield per unit of fishing effort. This is a true index
of stock and its decline shows the extent of reduction.

The figures available for plaice and cod taken from the North Sea
show much the same tendencies. Over a long period fishermen have
been afflicted by the consequences of the decline in yield per unit
effort indicated by such statistics. Already in the last century those
giving evidence before Royal Commissions expressed an uneasy feel-
ing that the profitability of the industry was declining. This situation
has been met by continual improvement in methods of fishing and the
exploitation of new grounds. The proportion of the total English
catch that is obtained from the nearer waters of the North Sea is now
much less than formerly, although the catch is no greater. We have
already seen that steam trawling and better gear all mean increased
labour for the crews, at greater distances from port. With all the
improvements in technique and discovery of new grounds we succeed
in obtaining from the sea little more fish than at the end of the last
century; and there is no greater profit for those engaged in the
industry.

The 'Great Law of Fishing', as Graham calls it, 'that fisheries that
are unlimited become unprofitable' has been tested on at least three
occasions. During the two Great Wars the intensity of fishing in the
North Sea was reduced and thereafter both of the expected changes
were seen : (a) fishing became more profitable, (b) there were found to
be more old fishes in the stock. Perhaps more encouraging is a case
where the intensity of fishing has been regulated not by war but by
law. The halibut fishery of the Pacific coast of North America showed
the typical history of increasing effort and decreasing yield. Fishermen
went farther and farther afield in larger and more expensive boats,
setting ever more and more lines, but yet brought home the same or
a smaller amount of fish. Thus in 1907 there were 1,800,000 sets of

xi REGULATION OF FISHERIES 289

lines used, in 1930, 6,400,000 sets, but instead of the 50 million
pounds of fish caught in the first year there were only 23 million
pounds in 1930! Then in 1932 a limitation of 23 million pounds was
imposed on the total catch allowed. Thereafter the stocks rapidly
increased and it was found possible to collect the standard catch in
five months instead of nine, with greatly increased profit.

Other attempts to regulate fisheries have been made; in particular
by the mesh regulations, designed to avoid taking small fishes. The
aim of regulation is nowadays not so much to save the stock from
undue reduction or extinction but rather to crop it in such a way as
shall make fishing profitable. Whatever we do it is unlikely that we
shall destroy all the stocks of any species, but there is reason to think
that the rate at which the stocks grow varies with the intensity of
fishing. If this is so, it may be possible to find an optimum that suits
both the fish and the fisherman.

In order to regulate a fishery effectively it is necessary to express its
characteristic parameters in a comprehensive equation. This has been
done by fisheries research workers who have provided mathematical
models such as are so often used in operational research (Beverton
and Holt in Graham, 1956). These equations show the effects that are
likely to follow variation in such a factor as the size of the mesh of the
cod end of the trawl net, which is one of the means used to regulate
a fishery. Fishing is a form of hunting, not of agriculture, and if we
cannot improve the yield by cultivation we may be able to do so by
working out the best way to fish.

Four primary factors are considered in the model, recruitment (R),
growth (W), mortality due to natural causes (M), and mortality due
to fishing (F). The relation of these factors to the yield by weight of
the fishery ( Yw) is considered and a theoretical equation for Yw is
derived. If the theory is correct the equation should be able to de-
scribe the yield of various fisheries in the past. It proves to do this
well and forecasts that improvements in yield could be obtained by
changing methods of fishing in the future. The data for testing the
theory come from statistics of the fishes caught, which give catches
per unit effort in each year class and their lengths. These are available
for several fisheries and we may consider the plaice in the North Sea
for the years 1929-38. Fish are said to be recruited when they first
enter the fished area of deeper water at 2-3 years old, being much less
than 1 per cent of the original batch of eggs. The value R for a given
mesh size is obtained from the number of fishes in the youngest
year class in the catch, with corrections to allow for the fact that

(29°)

300

200

g. 100

V X

Age-group

2000

1500

« 1000

500

o> 300

200

100

005 100 1-50

073 r

500r

400

50 100 150 200 250

Cod-end mesh size (mm)

Fig. 171A. Mortality rate of plaice. Natural logarithms of average number caught of each
age-group of North Sea plaice per 100 hours' fishing, 1929-38. The slope of the line gives
the estimate (F+M) = 0-83. The first three points are lowered by absence of fish from
the exploited area (some individuals still remaining in the nursery areas) and, possibly,

by rejection at sea.

Fig. 171B. Growth in weight of plaice. Average weight of fish of each age-group, 1929-38,
and the fitted von Bertalanffy equation for growth in weight.

Fig. 171c. Annual steady yield of plaice plotted against fishing intensity. Yield of plaice

per recruit (Y W IR) as a function of fishing mortality coefficient (F) with t p ' = 3-72 years,

corresponding to a 70 mm gauge mesh in trawls, double twine. The vertical line at F = 0-73

corresponds to the average pre-war fishing intensity.

Fig. 17 id. Effect of growth rate changing with density. The yield of plaice per recruit
(Y W IR) is shown as a function of mesh size with fishing intensity constant at F = 073,
but in calculating curve (b) the growth-rate was assumed to be reduced progressively as
the density of stock increases. The differences from the use of constant growth-rate, curve
(a), are considerable. Not only is the benefit from increase of mesh estimated to be less, but
the maximum yield is reached at a considerably smaller mesh size.

xi MORTALITY OF FISH 291

recruitment is not simultaneous or sudden. For the plaice in the North
Sea, with 70 mm mesh, R has been computed at 280 million fish for the
area considered, with mean age of 3 -7 years. A check from consideration
of numbers and mortality of eggs gave 320 million. Theoretically, we
also require to know the length of the life of the fish. Few plaice are
caught older than 15 years and almost none over 20 years. Since
there are very few in these older age-classes the upper limit is un-
important.

The coefficients of mortality M and F are estimated from the
numbers {N t ) of the original recruits R that survive at time t, N ( =
R e —M (t — t p ), where e is the natural base of logarithms and t p the
age at entry of the recruits. The total mortality (F-\-M) (due to natural
causes (M) and to fishing (F)) is estimated from the catches (Fig.
1 71 a). The part due to fishing alone is found by consideration of how
the catch varies when there are known differences in the fishing effort,
for example in the number of hours fished. In the extreme case, we
have the war-time periods, when there was no fishing. Confirmatory
evidence of the likelihood that a fish will be caught can be obtained from
marking experiments, giving the time between release and recapture.
For the plaice (F-\-M) has been estimated over the years 1929-38 as
0-83. This is the mean for all the age-classes together, though for
some purposes it can be calculated for each separately. That the rate
is indeed constant is shown by the close fit of Fig. 171 a. The first
three points do not fit because recruitment of these classes was still
incomplete. This method of treatment, in which the contributions of
year classes of the same age recruited in different years are considered
together, has the effect of averaging out this variation in recruitment,
which would be difficult to estimate.

The value of the natural mortality of plaice cannot be obtained for
these years from variations in fishing effort, since these were only
slight. However, since there was almost no fishing in the southern part
of the North Sea from 1940 to 1945, we can compare the age groups
V and VI of samples taken before the war with their surviving fellows
in the years after 1945. This gives a value for A/of o-i, and subtracting
this from 0-83 as the total mortality we obtain 073 as the mortality
due to fishing. Marking experiments give a value of 0-69, which is a
satisfactory agreement considering that the conditions were not en-
tirely similar. Moreover, the conclusions from marking involve other
problems, such as damage to the fish and rate of movement away
from the point of release. The conclusion that fishing is the most
important source of mortality in such areas is not new, but is obviously

292 FISHES AND MAN xi

of very great importance. If man is the chief predator, then change in
his activities will greatly influence the populations.

Knowing the number of fishes available and the rates at which they
are removed by natural causes and fishing in a given case, we still have
the even more difficult task of formulating the way in which the popu-
lation grows and then deciding whether some other method of fishing
would be more profitable. Probably there is a maximum total biomass
of fish of any given sort that can be supported in any area, determined
ultimately by the supply of inorganic salts. In the absence of fishing
this biomass is carried mainly in the form of large fish, whose presence
makes the growth of all fish in the population slow. The effect of fish-
ing is to remove mainly these larger animals, with a resultant increased
growth from all younger groups. The curve showing the relationship
between the yield per recruit and the intensity of fishing effort shows
a maximum (Fig. 171c). It should be possible to define a fishing mor-
tality rate at which the decrease in numbers is balanced by the incre-
ments in weight of the survivors.

There is every reason to hope that with further study of growth,
mortality, reproductive potential, and utilization of food by fish the
yield could be increased and the effort of getting it reduced, making
fishing more profitable to the fisherman and providing the maximum
amount of food. At present the economic conditions and psychology
of the fishing populations interact with the factors limiting the stocks
and the growth of the fish to produce a complicated system of inter-
relations that is unstable and unsatisfactory to all parties.

The increase in weight of the population is perhaps the most diffi-
cult feature of the pattern to express mathematically. Weight plotted
against age shows an asymmetrical sigmoid shape, with an inflexion
(Fig. 171B). The curve fitted is arbitrarily chosen, being that deduced
from the hypothesis of Bertalanffy, that the weight is subject to
opposing forces of anabolism and catabolism, taken as proportional to
the absorbing surfaces, that is, to the squares of the linear dimensions.
As before, the fit is poor for the lower points, probably because there
are incompletely recruited classes. Elsewhere the fit is good but the
important point for us is the inflexion, since it indicates that the
growth-rate decreases in the later part of life. The older plaice are
from this point of view inefficient in providing more biomass. Fur-
ther, the longer a fish has to be kept alive in the sea before it is eaten,
the more of the limited raw materials are devoted to this end and the
less to providing human food. With present methods it is not possible
to give full weight to all of these factors in deciding what is the best

xi YIELD EQUATION 293

way to fish. However, the theoretical equation derived by Beverton
and Holt gives us the yield Y w in terms of the parameters already
discussed with in addition the maximum weight W^ and a factor K
related to the catabolism

d ^ = FN l W. (1)

The number N t at the time t is given by

N t = R^F+MXt-t,^ ( 2 )

and the weight W t by

W t = W^i-e-w- 1 *?). (3)

This last is best handled as a cubic of the form

W t = W^2 Q -n e ' UK(l - tti) -
n =

Substituting (2) for N t in (1), and (3) for W t we obtain

at ri=o

This provides the basic equation with which forecasts of effects of
changing the various factors are made.

Empirical values can be obtained for the yield per recruit (Y W I R )
for various values of F, with a mesh of 70 mm. Such a yield/intensity
curve of North Sea plaice is shown in Fig. 171c. The graph shows that
with infinite effort all fish would be caught at recruitment and would
yield their initial weight of 123 g. At the pre-war fishing mortality of
0-73 the yield was 200 g. But the curve has a clear maximum at over
250 g, with a fishing mortality of only 0-22. Therefore if these pre-
dictions are correct, a lesser intensity of fishing should provide a
greater yield.

One possible way of reducing fishing intensity is to increase the
size of the mesh of the cod net. If the age at recruitment were in-
creased to ten years the yield per recruit would be as high as 400 g
(Fig. 17 id, curve a). Beyond this maximum, the yield falls because of
the death of fish by natural causes before entering the exploited phase.
However, this curve assumes that the growth-rate is independent
of density and it ignores the complex problem of the competition of
old and young fishes for a limited supply of raw materials. Curve b
of Fig. 17 id has assumed a reduced growth-rate with increasing
density and it will be seen that the advantage of increasing mesh size
is much reduced.

(294)

500

400

^ 300

200

100 •

500

400

300-

>T* 200-

100

\ c

\ J£-

, '

/\ /
I \ '

If ! -\X b)

/ A X(cK

Running costs

zp\~-

FlG. 172A. Annual steady yield of plaice plotted against mesh at various fishing intensities.

The yield per recruit ( Y W \R) as a function of t p ' for various values of F, to show how the

height and location of the maximum changes with F.

Fig. 172B. Eumetric Yield curve for plaice. If a change of mesh accompanies a change in
fishing intensity in such a way that each value of F is matched by the mesh that would
give the maximum steady yield at that value, the resultant curve of steady annual yield
per recruit (Y w jR) for plaice differs widely from that of Fig. 171c, particularly in having

no maximum.

Fig. 172c. An exercise in bionomics. Curve (a) is a eumetric curve in which steady yield
instead of being expressed in weight is now in money value, which is plotted against the
economic equivalent of intensity of fishing, namely, running costs. From those are derived
(6) the annual profit and (c) the profit expressed as a rate on running costs, which in many
situations bear a constant relation to capital outlay.

MP = maximum profit point; ZP = zero profit point.

xi CONTROL OF FISHING 295

In practice it is much more economical to reduce the fishing mor-
tality by lowering the number of hours fished than by increasing the
mesh size. We require, therefore, to know the optimum mesh size for
each level of fishing effort. This we can obtain by plotting, as in Fig.
1 72 a, a series of yield/mesh curves for different sizes of mesh, that
is, ages of recruitment t p . From the maximum of these, plotted against
the corresponding fishing mortality, we obtain Fig. 172B, known as
the eumetric yield curve. This shows an increasing yield towards an
asymptote as fishing increases, but without a maximum.

Evidently the greatest yield is obtained at the highest fishing inten-
sity, but this could be achieved only at a prohibitive cost. In order to
obtain the greatest possible yield, we have to consider the cost of unit
effort of fishing and the value of the yield. This has been done, making
certain assumptions, in Fig. 172c. Here the eumetric yield curve is
expressed by plotting value of catch against running costs. Another
line shows the profit (total value minus total cost) whose maximum
might be said in one sense to be the 'best' level of fishing. This curve
also crosses the x-axis, where there is no profit in fishing — -this being
the condition which an uncontrolled fishery tends to approach.

Of course the actual 'best' level of fishing for any given situation
may be affected by many social and political factors. However, from
studies such as these it begins to be possible to understand the vari-
ables that are affecting a fishery and to express them precisely. The
value of such work is shown by the fact that international regulation
of some fisheries has been agreed. For example, since 1954 the white-
fish populations of the North Sea have been regulated by control of
the size of mesh used for fishing.

XII

TERRESTRIAL VERTEBRATES: AMPHIBIA

1 . Classification

Class Amphibia

*Subclass i. *Stegocephalia. Devonian-Trias
Order i. *Labyrinthodontia. Devonian-Trias
Suborder i. *Ichthyostegalia. Upper Devonian

*Ichthyostega; *Elpistostege
Suborder 2. *Embolomeri. Carboniferous

*Eogyrimis; *Loxomma
Suborder 3. *Rhachitomi. Carboniferous-Triassic

*Eryops, Lower Permian ; *Cacops, Lower Permian
Suborder 4. # Stereospondyli. Triassic

*Capitosaurus, Upper Triassic; *Buettneria, Upper Triassic
Order 2. *Phyllospondyli. Carboniferous-Lower Permian

*Bra?ichiosaurus, Lower Permian
Order 3. *Lepospondyli. Carboniferous-Permian

*Dohchosoma, Carboniferous ; *DipIocaulus, Permian ; *Micro-
brachis, Permian
Order 4. *Adelospondyli. Carboniferous-Lower Permian
*Lysorophns, Carboniferous
Subclass 2. Urodcla (= Caudata). Jurassic-Recent

Molge; Salamandra; Ambystoma; Necturus
Subclass 3. Anura (= Salientia). Carboniferous-Recent
*Miobatrachus; *Protobatrachiis ;
Rana; Bufo; Hyla; Pipa
Subclass 4. Apoda (= Gymnophiona = Caecilia). Recent
Ichthyophis; Typhlonectes

2. Amphibia

During the later part of the Devonian period a population of lung-
fishes lived in the pools and there is every reason to suppose that some
of these animals, first crawling from pool to pool and then spending
more time on the land, gave rise to the terrestrial populations that
we distinguish as amphibia. No doubt the early efforts at land life
were crude. The whole locomotory and skeletal system comes under
a completely new set of forces when the support of the water is with-

xii. 1-2 AMPHIBIA 297

drawn and the effects of gravity become insistent. At the same time
the skin must be changed to resist desiccation, the respiratory system
adapted to use gaseous oxygen, the receptors to signal the strange new
configurations of stimuli. It is not surprising that these new conditions
produced greater changes in vertebrate organization than had occurred
in tens of millions of years previously. Nevertheless, so slow is the
pace of evolution, the only known Devonian amphibia, and many of
the Carboniferous ones too, still looked and presumably behaved very
like fishes. Animals of this sort (e.g. *Eogyrinus) floundered about on
land for 30 million years or more before producing definitely terrestrial
types such as the Permian *Eryops.

Of all the features that arose at this time in connexion with the new
life on land the presence of pentadactyl limbs is perhaps the most
conspicuous. It is appropriate that this should be marked in zoological
nomenclature: the amphibia are the first of the great group of land
vertebrates, the Tetrapoda.

All existing amphibia have been much modified since their Devonian
ancestry, yet they retain many features that show how the transition
from water to land was produced. These modern forms are by
no means a precariously existing remnant but are quite numerous
and successful in the ecological niches that they occupy; they form
an important element in many food chains. There are some 2,000
species at present recognized, placed in 250 genera. However, con-
trasting this with the numerous species of teleosts, of birds, and of
mammals we shall see that the amphibians, though well adapted for
certain situations, do not succeed in maintaining themselves in many
different types of habitat. Broadly speaking they are unable to survive
for long except in the proximity of water. There are desert toads, such
as Chiroleptes of Australia, but these survive by burrowing and by
special abilities, such as the power to hold large amounts of water,
associated with loss of the glomeruli of the kidneys.

Modern amphibia belong to three sharply separated subclasses.
Urodela (newts and salamanders) retain the original long-bodied,
partly fish-like form. The Anura (frogs and toads) have lost the tail
and become specialized as jumpers. The Apoda are limbless, blind,
burrowing animals found in the tropics. The urodeles and anurans
are found as fossils back to the Cretaceous and Trias respectively, but
we have only scanty information about their connexion with the
earlier amphibians, which are grouped loosely together as the Steno-
cephalia. These are found in rocks about 275-160 million years old,
that is to say from the late Devonian to the Trias (Fig. 211).

298 AMPHIBIA xii. 3-

3. The frogs

Perhaps the most successful of all amphibia are those belonging
to the genus Rana, abundant in every part of the world except in
the south of South America, on oceanic islands, and New Zealand.
Ranid frogs are typical of the highly specialized subclass Anura, whose
members usually inhabit damp places such as marshes or ditches,
living for most of their life in the grass or undergrowth and feeding by
catching flies and other insects with their tongue. They are preyed
upon by birds, fishes, and especially snakes, and escape from these by
their hind legs, used either for jumping or swimming. The young
develop as tadpoles in the water, where they are omnivorous. The
various species differ in size and small points of colour, though there
are also some that depart widely from the usual habits, e.g. R. fossor
which burrows. R. temporaria is the species found in Great Britain,
R. esculenta is a slightly larger form found on the continent of Europe
and occasionally in east England, R. pipiens is the common small
North American frog; R. catesbiana the giant bull-frog, whose body
is up to 9 in. long, also lives in North America. R. goliath of the
Cameroons is over a foot long, but is mainly aquatic.

4. Skin of Amphibia

The earliest amphibia possessed the scales of their fish ancestors,
but these were soon lost in most lines, though retained in some
Apoda; perhaps they were too heavy to be worth while for creatures
contending for the first time with gravity, unaided by water. Some
frogs carry dermal plates on the back, however, fused to the neural
spines (Brachycephahis of Brazil). Amphibia differ from reptiles in
that the skin is moist and used for respiration; on the other hand, the
skin also shows a character typical of land animals in having heavily
cornified outer layers. The epidermis therefore consists of several
layers in the adult frog and is renewed at intervals by a process of
moulting. The moult is under the control of the pituitary and thyroid
glands and does not occur if either of these be removed, the kera-
tinized cells merely accumulating in those circumstances as a thick
skin. Local thickenings of the epidermis often occur in amphibia, for
instance to form the horny teeth by which the larva feeds. Such thick-
enings are also a conspicuous feature of the warty skin of the toads
(Bufo), which mostly have a drier skin and are more fully terrestrial
than are the frogs. The fact that the epidermis of amphibia can pro-
duce local thickenings is of interest in considering the origin of
feathers and hairs. In larval amphibians the skin is ciliated.

xii. 5 SKIN OF AMPHIBIA 299

The glands of the skin are more highly developed than in fishes,
and are of two types, mucous and poison glands. Both of these consist
of little sacs of gland-cells, derived from the epidermis. The mucus
serves to keep the skin moist, this being essential if the skin is to
respire; the secretion may perhaps also serve for temperature regula-
tion. The problem of regulation of temperature is important for all
terrestial animals, since air conducts heat much less well than water
and therefore violent changes of temperature are met. Evaporation
produces large influences on temperature and no doubt it was the
adjustment of these effects that led to the development of temperature-
regulating mechanisms in birds and mammals. Frogs in dry air are
always found to be colder than their environment, the difference
being sometimes as much as 5 C. It is probable that in some cir-
cumstances use is made of this cooling, since tree-frogs (Hyla) may
be found fully exposed to tropical sunlight, which would be expected
to raise their temperatures to a lethal level. On the other hand, the
loss of water involved by evaporation in this way would presumably
soon become serious.

The poison glands or granular glands are less developed in Rana
than in Bufo ('the envenom'd toad') where they are collected into
masses, the parotoid glands. The effect of the poison on man is to
produce an irritation of the eyes and nose; only rarely does it affect
the skin of the hands. When swallowed it produces nausea and has
a digitalis-like action on the heart. The poison of Dendrobates of
Colombia is used on arrows; it acts on the nervous system.

Some amphibia have characteristic smells, produced by secretions,
and these are probably used to attract the sexes to each other. In
some male newts (Plethodontidae) there are special collections of these
gland-cells below the chin.

Another use of glandular secretions is to keep the eyes and nostrils
free from obstruction. The demands of terrestrial life require the
production of numerous such special devices and lead to the com-
plexity that we recognize as an attribute of these 'higher' animals.

5. Colours of Amphibia

The use of colour is also highly developed in amphibia. The
animals are often greenish and the colour is produced by three layers
of pigment cells, melanophores lying deepest, guanophores, full of
granules, which by diffraction produce a blue-green colour, and yellow
lipophores, overlying these and filtering out the blue. Change of colour
is produced by expansion of the pigment in the melanophores under

300

AMPHIBIA

xii. 5

the action of the secretion of the pituitary gland (Fig. 173). Move-
ments in the other chromatophores can also affect the colour, yellow
being produced by disarrangement of the guanophores and so on.
Other colours may contribute to the patterns, blue (though rarely)
by the absence of the lipophores, red by pigment in the lipophores.
Changes in the melanophores may be of two sorts, primary or
direct and secondary or visual. The primary response depends on the

Fig. 173. Stages of dispersal of pigment in the melanophores in the web of

the frog Xenopus, as used by Hogben to assess the melanophore index.

(After Hogben and Slome, Proc. Roy. Soc. B. 108.)

direct effect of light on the skin, causing expansion. The secondary
effect consists in contraction of the pigment if the animal is illumin-
ated on a light-scattering surface (light background) but expansion
(and hence darkening of the animal) when it is illuminated from above
on a light-absorbing (dark) background. There are, therefore, distinct
responses from different parts of the retina. Illumination of the dorsal
part produces contraction, of the ventral part expansion of the
melanophores.

Hogben and his co-workers have shown that the control of the
colour change of amphibians is mediated by variation in the secretion
of the pituitary gland ; there is no direct nervous control of the melano-
phores. There is still some doubt whether the pituitary produces its
effects by means of one hormone or two. The most fully known in-
fluence is that of the posterior lobe, producing a B substance, also
known as intermedin, which makes the melanophores expand. Ex-

xii. 5

COLOUR CHANGE IN AMPHIBIA

301

tracts of the pituitary of mammals (or other vertebrates) produce this
effect when injected into frogs, and after removal of the pituitary a
frog becomes pale in colour. There is also some evidence for secre-
tion bv the anterior lobe of a W substance that causes paling. After
removal of the whole pituitary the melanophores are found to be not
in the wholly contracted stage 1 of Hogben's melanophore index (Fig.
173) but in a state (stage 2 or 3) intermediate between this and full
expansion (stage 5). If, however, the posterior lobe alone is removed
the animal becomes completely pale (stage 1). This certainly suggests

10 12 14
Hours

Fig. 174. Effect of an extract containing the b (melanophore-expanding) substance on

three groups of Xenopus. All were of the same weight and received the same dose.

A, whole pituitary removed; D, intact animals; c, posterior lobe only removed.

(From Waring, after Hogben and Slome.)

the secretion of a W substance by the pars anterior. There are also
differences in the response to injection of B-containing extracts after
total and partial removal of the pituitary (Fig. 174). The position is
complicated by the fact that extracts of mammalian pineal or adrenal
medulla will cause contraction of amphibian melanophores, though it
is uncertain whether these effects have any physiological significance.

In amphibia there is no direct control of the pigment cells by
nerve-fibres such as are present in bony fishes (p. 259). The colour
change is therefore rather slow. After removal of the pituitary the
melanophores still show slight changes correlated with change of in-
cident illumination, indicating a small degree of direct response as
independent effectors. Temperature and humidity also influence the
colour in many amphibia. In frogs contact with water accentuates the
black-background response and in darkness produces expansion. On
the other hand, drying induces contraction of the melanophores, even
upon a black background.

The colour patterns adopted are usually cryptic or concealing in
their effect, but the colour also has an important influence on the
temperature and varies with it and with the humidity, as well as with
the incident illumination. The uniform brilliant green of tree-frogs

3 o2 AMPHIBIA xii. 5-

makes them very difficult to see among the leaves; on the other hand,
R. temporaria and other species living among grass show a pattern of
dark marks, which breaks up their outline. In other amphibians, how-
ever, the colour makes the animal
conspicuous, for instance the
black and yellow markings of
Salamandra maculosa. Conspi-
cuous colour is often associated
with great development of the
poisonous parotoid glands and
is therefore presumably sematic
or warning coloration, allowing
recognition by possible attackers.
This correlation is not always
found, however; the toad Cera-
tophrysamericanaisd\i\\co\o\irtd
but poisonous, whereas C. dor-
sata has a bright pattern but is
harmless.

Many frogs make a sudden
exposure of brightly coloured
patches on the thighs when they
jump. This presumably serves
to startle the attacker and such
colours may be called dymantic
or startling. A similar use of
colour is made by the cuttle-
fish (Sepia), which may suddenly
produce two black spots when
alarmed, and also by some Lepi-
doptera. It is interesting that the
colour used in this way so often
takes the form of black spots
('eye-spots'), which have an es-
pecially striking quality. In some anurans these colours are irregular
dark marks, but in Mantipus ocellatus they take the form of definite
'eye-spots'.

It must not be forgotten that the presence of pigment serves to
protect the organs from the effects of light, which may cause contrac-
tion when it falls directly upon muscles. Dark colour may also assist
in the absorption of heat, both in the adults and in the eggs.

(a) (b)

Fig. 175. Record of the movements of
Ambystoma walking on a smoked drum,
a, in rapid locomotion (with the body on
the ground); b, in slow locomotion (raised
up on the legs). (From Evans, Anat. Rec.
95.)

xn. 6

(3°3)

6. Vertebral column of Amphibia

The general build of the body is essentially fish-like in stegocepha-
lian and urodele amphibians. Such forms have two means of locomo-
tion. When they are frightened and move fast they wriggle along with
the belly on the ground, the effective agent being serial contraction
of the segmentally arranged myotomal musculature, by means of which
the animal as it were 'swims on land', with the legs hardly touching
the ground (Fig. 175). When moving deliberately, on the other hand,

Fig. 176. Drawings made from photographs of a newt (Triturus)
in slow locomotion. (After Evans, Anat. Rec. 95.)

a newt raises up its body on the legs, which then propel it along as
movable levers, the main part of the action being produced by drawing
back the humerus or femur, the more distal muscles of the limbs
serving to maintain the digits pressed against the ground (Fig. 176).
The carrying of the weight on four legs places an entirely new set
of stresses on the vertebral column. Instead of being mainly a com-
pression member as it is in fishes it comes to act as a girder, carrying
the weight of the body and transmitting it to the legs. This new
function produces a column whose parts are largely bony and articu-
lated together, flexibility becoming less important than strength. The
new types of strain involve new muscle attachments and the develop-
ment of special processes and parts of the vertebrae (p. 307). These
changes, however, have not proceeded very far in the amphibians;
many urodeles spend much time in the water and their vertebrae often
show a lack of ossification, parts of the notochord persist and provide
the main compression member required for swimming.

3°4

AMPHIBIA

xii. 6

In the anurans the entire skeletal and muscular system has become
specialized for the peculiar swimming and jumping methods of loco-
motion, by means of extensor thrusts of both hind limbs, acting

Fig. 177. Reflexes associated with the transition from swimming to walking in toads.
The shaded outlines show successive positions as the animal emerges on to solid ground.
The first effective contact is by the left fore-limb whose retraction and extension
elicits a crossed protraction reflex in the right fore-limb (Lj), a diagonal extensor
response in the right hind-limb (L 2 ), and a placing response in the left hind-limb (L 3 ).
The right fore-limb then touches the ground and produces corresponding responses
Rx- 3 . The left fore-limb in response to stretch of its protractor muscles swings forward
and this produces retraction of the left hind-limb (L 4 ) and protraction of the right
hind-limb (L 5 ). Fixation of the right hind foot then produces a crossed flexor response
(RHJ. (From Gray, J. exp. Biol. 23.)

together. Frogs, and especially toads, also walk on land, bringing into
play a set of myotactic (proprioceptor) reflexes that depend on the
contraction of the muscles against an external resistance (Fig. 177).

The actions of jumping and walking are possible because of pro-
found changes in the arrangement of the skeleton and muscles. The
myotomal muscles no longer perform their primitive function of pro-
ducing metachronal waves of contraction, and accordingly the verte-
bral column (Fig. 178) has lost its original flexibility. Instead, it is

xii. 6

VERTEBRAL COLUMN

305

Fig. 178. The skeleton of the frog, seen from the dorsal surface; the left
suprascapular and scapular have been removed.

a. astragalus; c. calcaneum; d. suprascapular; e. exoccipital ; /. femur;//), frontoparietal;
g. metacarpals; h. humerus; i. ilium; k. metatarsals; /. carpus; m. maxilla; w. nasal; o. pro-
otic; p. pterygoid; pm. premaxilla; q. 'quadratojugal'; r. radio-ulna; J. squamosal; se.
sphenethmoid; s.v. sacral vertebra; t. tibio-fibula; u. urostyle.
(After Marshall, The Frog, Macmillan.)

attached to the pelvic girdle and acts as a support by which the
movement of the hind limbs is transmitted to the rest of the body.
There is no longer any sinuous motion and the number of vertebrae
is very low (nine in the adult Ra?ia), and behind them is an unseg-
mented rod of 'hypochordal' bone, the urostyle. Shortening of the
body is a characteristic feature of the change from aquatic to terrestrial

(3o6)

Fig. 179. Transformation of crossopterygian pectoral girdle and fin into
pentadactyle limb. Oblique front view of left side.

a, *Eusthenopteron\ b, *Eogyrinus; c, *Eryops; clt. cleithrum; civ. clavicle;

h. humerus; p. pubis; sc. scapula; s.cl. supracleichrum. (Modified from

Gregory and Raven, Ann. N.Y. Acad. Sci. 42.)

Fig. 180. Transformation of crossopterygian pelvic fin into tetrapod limb.

a, *Eusthenopteron; B, hypothetical; c, *Trematops. f. femur; fi. fibula; il. ilium;
is. ischium; t. tibia. (Modified from Gregory and Raven.)

xii. 6-7 AMPHIBIAN LIMBS 307

life, and is seen in many lines of amphibian and reptilian evolution.
It has proceeded farther in the frogs than in any other tetrapods.

The second to eighth vertebrae of Rana are concave in front, con-
vex behind (procoelous), and have large transverse processes. In other
amphibians they may be amphicoelous or opisthocoelous. They fit
together by complex zygapophyses. The first vertebra has two con-
cave facets for articulation with the two condyles of the skull; its
centrum and transverse processes are much reduced. The ninth

Fig. 181. Diagrams illustrating the probable changes in position during the
evolution of a pelvic fin into a tetrapod limb. A as in Ceratodus; B, double
flexure to give knee and ankle joints, leaving foot direct backwards; c and
D, rotation of tarsus and digits turning foot forward. (From Gregory and
Raven, after Romer and Byrne.)

(sacral) vertebra has large transverse processes, which articulate with
the ilia of the pelvic girdle. There are free ribs in the primitive frogs
Ascaphus and Leiopelma.

7. Evolution and plan of the limbs of Amphibia

The girdles of the paired limbs have become much changed from
their fish-like condition (Figs. 179 and 180). Their basic pattern is
similar in the two limbs and has been retained throughout the w r hole
tetrapod series. Whereas in fishes the girdles are rather small carti-
lages and bones, the pelvic girdle being restricted to the ventral region
of the body, in amphibians they become enlarged in connexion with
the w T eight-bearing function of the limbs.

The details of the sequence of stages by which a tetrapod limb
arose from a fish fin are still somewhat disputed. It is probable that
the ancestral crossopterygian possessed a lobed fin, rather like that
seen in *Eusthenopteron (Fig. 179). As the fishes came on land the fin

3 o8 AMPHIBIA xn. 7-

would be used as a lever, giving greater effect to the wave-like motions
by which the creature 'swam on land'. The muscles of the limb, con-
tracting in a serial manner, would tend to move it backwards and
forwards relative to the body, thus assisting in locomotion. At first
the limb perhaps carried only little weight, but as tetrapod evolution
proceeded the limbs became elongated and turned under the body,
raising it off the ground. To work effectively in this way the limbs
came to be held bent down at elbow and knee (Fig. 181) and a firm
application to the ground was produced by bending outwards at
wrist and ankle. Finally the limbs were brought in to the side of the

Fig. 182. Suggested protetrapod stage, between crossopterygian and labyrinthodont.
(From Oregon - and Raven.)

body by rotation, such that the elbow pointed backward and the knee
forward.

These are the changes that must have occurred at some time to
produce the full tetrapod condition, but we cannot follow exactly the
order in which they took place. Their effect is to convert a paddle-
like fin, whose main movements were up and down, and were used
for stabilization in the horizontal swimming plane, into an elongated
jointed strut, on which the animal can balance, and which can be
moved as a lever to produce locomotion.

The limbs and girdles and their muscles show a remarkable con-
stancy of pattern throughout the tetrapods. The muscles of the fins of
fishes are concerned mainly with lowering and raising (Fig. 192), and
they run from a girdle in the body wall to the basal radials in the fin,
and between the radials. After the animals came on land the muscles
served not only to raise and lower the limbs but also to draw them
forwards and backwards; indeed, many fishes already make such
movements, including Protopterns. The muscles therefore become
arranged around the shoulder and hip joints into groups serving as
adjustable braces, by which the body is balanced on its legs and by
whose contraction the latter are moved. Those muscles that draw
the limb towards and away from the mid-ventral line can be called

xii. 8 SHOULDER GIRDLE 309

medial and lateral braces (adductors and abductors) and the muscles
drawing the leg backwards and forwards are posterior and anterior
(retractor and protractor) braces. For the attachment of these muscles
proximally the pectoral and pelvic girdles, small in fishes, become
expanded into plates (Figs. 180 to 182), and these are divided into
a number of characteristic pieces, though the mechanical reason for
the division is not clear.

8. Shoulder girdle of Amphibia

The earliest labyrinthodonts (e.g. *Eogyrinus) inherited a shoulder
girdle almost exactly like that of their osteolepid ancestors except that
a new dermal element, the interclavicle, was added to the ventral
surface. Although the presence of a sternum has never actually been
recorded, it is generally assumed that a cartilaginous structure of this
type was present between the hindermost margins of the epicoracoid
cartilages. As in gnathostomes generally (except elasmobranchs) the
shoulder girdle was a dual structure consisting of (a) a primary or
endochondral component evolved from the basal fin elements of the
ancestral fish form and serving to provide an articulatory surface for
the limb as well as points of attachment for the limb musculature, and
(b) a dermal ring of bony elements (skin scales) which had sunk
inwards and applied themselves to the ventro-anterior surfaces of the
endochondral girdle which, consequently, they braced and supported.

The endochondral girdle consisted of two half rings, which over-
lapped in the ventral midline. Each half was a single unit but, by
topographical comparison with girdles of later tetrapods, it is often
arbitrarily divided into two regions, a dorsal scapula and a ventral
coracoid. Between these two regions a screw-shaped glenoid received
the humerus. The one endochondral ossification is usually homo-
logized with the scapula of amniotes (Watson, 191 7). Later forms
(e.g. * Seymonria, *Diadectes) possessed a second bony element which
is generally interpreted as a precoracoid. The endochondral girdle was
small in the earliest amphibia (e.g. *Eogyrinus). In later genera its size
progressively increased, presumably to withstand the greater thrust
transmitted by the larger limbs of these forms and to provide attach-
ment for the increased mass of brachial musculature.

The dermal girdle consisted, typically, of paired cleithra, clavicles,
and interclavicle. The latter, a new element, lay between and often
beneath the clavicles and, together with the sternum, probably formed
a locking mechanism preventing the complete separation of the epi-
coracoid cartilages. In the earliest rhachitomes (e.g. *Eogyrinus) the

310 AMPHIBIA xii. 8

dermal girdle was attached to the post-temporal region of the skull,
as in bony fish. This connexion was soon lost in later forms, pre-
sumably to permit greater mobility of the head. This foreshadowed
the reduction and loss that was the subsequent fate of the dermal,
shoulder girdle elements in tetrapod evolution.

Of the modern amphibia, the Salientia most nearly approach the
condition of the fossil forms and they, alone, of recent tetrapods, have
retained a cleithrum. Each half of the endochondral girdle consists
of a dorsal, bony scapula with a cartilaginous suprascapula, and a
ventral coracoid bone connected to an anterior precoracoid cartilage
by a mesial epicoracoid cartilage. The precoracoids are invested by
the clavicles and, as in all modern amphibians, the interclavicle is
absent.

Anuran shoulder girdles may be divided into two broad categories
according to whether the two epicoracoid cartilages are fused mesi-
ally (a) along their entire lengths (firmisternal condition) or (b) along
their anterior edges only (arciferal girdles). The latter occurs typically
in 'walking', toad-like Anura (e.g. Bufonidae, Pelobatidae) and in the
aquatic xenopids. The clavicles are the main struts for keeping the
glenoids apart and, consequently, they are well developed and never
lost. The coracoids, on the other hand, may only be moderately well
developed. Immediately behind their point of fusion the epicoracoid
cartilages diverge and overlap and their posterior margins are con-
tinued as epicoracoid horns, which run in lateral grooves on each side
of the sternum. The posterior tip of each horn has a muscle attach-
ment connecting with abdominal recti. This type of sternum/epi-
coracoid system permits a certain degree of independent movement of
the girdle halves whilst, at the same time, preventing the epicoracoid
cartilages from being forced too far apart. The mechanism clearly
facilitates the independent arm movements characteristic of locomo-
tion in the arciferal frogs.

The firmisternal girdle is a rigid structure allowing no independent
movement of the two halves (Fig. 183). It occurs typically in frogs
with a jumping habit (e.g. Ranidae, Microhylidae) and provides an
excellent landing mechanism. The glenoids are braced apart by the
large coracoids. The clavicles and precoracoids are thus deprived of
their strutting function and frequently become reduced or even com-
pletely lost. No epicoracoid horns are present and the sternum, no
longer involved in locking the girdle halves, serves principally for the
attachment of pectoral muscles. This function is also performed, in
some frogs, by a prezonal (omosternal) element, which is really an

(3ii)

FROG

TOAD

Fig. 183. Amphibian pectoral girdles.

b. precoracoid bridge; c. coracoid; cl. clavicle; c.p. coracoid process; c.t. cleithrum; d.b.
dorsal blade; e.l. precoracoid cartilage; e.m. epicoracoid muscle; g. glenoid; g.f. glenoid
fossa; /;. epicoracoid horn; i.cl. interclavicle; /. left epicoracoid cartilage; pc. prezonal
cartilage; p.o. prezonal bone; po.t. posterior temporal; r. epicoracoid cartilage; s. sternum;
sc. scapula; sk. scapulo-coracoid ; s.o. sternal bone; s.r. ventral blade; ss. suprascapular
cartilage; st.c. sternal cartilage; su. coraco-cleithral suture; sup.ct. supra-cleithrum.

312

AMPHIBIA

xn. 8-

extension of the precoracoid cartilages. This structure, although
present in some arciferal girdles (e.g. Leptodactylidae), is more usually
associated with the firmisternal pattern and a jumping habit.

The shoulder girdles of modern urodeles are greatly simplified, the
only ossification being a scapulo-coracoid encircling the glenoid. The
two epicoracoids overlap broadly, and anteriorly are quite free of
each other; posteriorly they are usually rather weakly locked by a

LEPTODACTYLUS

Fig. 183(a). Leptodactylus pragnathus. Ventral view showing sternal articulation with
girdle. The left half of the ventral sternal blade has been removed. Labelling as in Fig. 1 83 .

cartilaginous sternum. The Apoda, of course, retain no vestiges of
either limbs or limb girdles.

9. Pelvic girdle of Amphibia

The pelvic girdle is much larger in land animals than the small
ventral cartilages found in fishes. It is formed of three main cartilage
bones in all tetrapods (Fig. 184), but it is not clear how these origin-
ated, nor whether the division has mechanical significance. The dorsal
ilium becomes attached to specially modified transverse processes of
one or more sacral vertebrae. This ilium can be regarded mechanically
as the ossification along a line of compression stress due to the weight-
bearing.

The ventral portion of the girdle consists of an anterior pubis and
posterior ischium, the three bones meeting at the acetabulum, where

XII. IO

PELVIC GIRDLE

313

the femur articulates. The girdle thus provides a plate to which the
muscles that brace the limb can be attached in such a way as to
balance the body on the leg.

In urodeles the pelvic, like the pectoral, girdle becomes reduced and
mainly cartilaginous. The pelvic girdle of anurans is highly specialized
and unlike that of any other vertebrate. The ilia are very long and
directed forward to articulate with the transverse processes of the single
pair of sacral vertebrae. The base of the ilium is expanded to make the

ac. Cryptobranchus

is. it- %

Eryops

Necturus p.

Iguana

Fig. 184. Pelvic girdles of lower tetrapods. Regions mainly cartilaginous are stippled.
ac. acetabulum; /'/. ilium; is. ischium; of. obturator foramen; p. pubis. (After Evans.)

dorsal portion of a disk, of which the pubis is the anterior, the ischium
the posterior part, with the acetabulum at the centre. The girdle is
thus developed into a long lever for transferring force from the limb
to the vertebral column during jumping.

Considerable movement is possible at the ilio-sacral joints, at least
in Salientia (Whiting, 1961). In Rana the ilia may rotate through an
angle of over 90 on the sacral ribs in the vertical plane. This move-
ment is used during a strong leap. In Discoglossus the sacrum can be
turned laterally on the pelvis through 20°. The movement is used both
in turning to take food and in locomotion. In Xenopus the sacrum
can slide backwards and forwards on the pelvis, producing a con-
siderable shortening and lengthening of the whole animal. This
movement is probably used in driving into the mud.

10. The limbs of Amphibia

The pattern of bones and muscles in fore and hind limbs of tetrapods
is surprisingly constant in spite of the various uses to which the limbs

3'4

AMPHIBIA

XII. 10

are put. Evidently similar morphogenetic processes are at work in
both limbs. There are nearly always three main joints in each limb,
at shoulder (hip), elbow (knee), and wrist (ankle). The hand and foot
provide basically similar five-rayed levers, with several joints in the
digits (Figs. 185 and 186).

The bones of the limbs can be plausibly derived from those of a
crossopterygian fin, and indeed the condition in *Eusthenopteron
already distinctly suggests that of the limb of an early amphibian (Figs.
179 and 180). We know less about the origin of the hind than of the
front leg, but the two are so similar that they may be treated together
for elementary analysis. There is a basal humerus (femur), articulating
distally with two bones in each case, a more anterior (pre-axial) radius
(tibia) and a posterior (post-axial) ulna (fibula). These bones articu-
late at the wrist or ankle with a carpus or tarsus, consisting, in the fully
developed condition, of three rows of little bones, namely 3 in the
proximal row, about 3 centrals, and 5 distals. Each of the latter carries
a digit, composed of numerous jointed phalanges. In naming these
bones of the carpus and tarsus it is convenient to call the proximal
carpals by their position radiale, intermedium, and ulnare and the
tarsals tibiale, intermedium, and fibulare. The centrals and distal
carpals may then be numbered beginning with 1 at the pre-axial
border in each case. Unfortunately other less explicit systems of
naming are in use, as shown in the following table.

Plan of the Tetrapod Carpus and Tarsus. {The names used for the bones
in man are shown in brackets.)

Carpus

Pre-axial

Post-axial

Proximal

radiale (scaphoid)

intermedium
(lunate)

ulnare (triquetral)

Central

centrale (tubercle
of scaphoid)

Distal

carpal i

4 and 5

(trapezium)

(trapezoid)

Tarsus

(capitate)

(hamate)

Pre-axial

Post-axial

Proximal

tibiale (talus or
astragalus)

intermedium (os
trigonum)

fibulare (calcaneum)

Central

centrale (navicular)

Distal

tarsal i

4 and 5

(medial cuneiform) (intermediate

(lateral cuneiform)

(cuboid)

cuneiform)

The plan of the carpals and tarsals can well be imagined to have been
derived from that of a fin such as is seen in the fish *Eusthenopteron
(Fig. 179), which might be said to have humerus, radius, and ulna,

(315)

^•^ Nee tar us
Cryptobranchus

Fig. 185. Front legs of various lower tetrapods.
H. humerus; R. radius; u. ulna. (Modified from Evans, J. Morph. 74.)

1 m w

Trematops

Cryptobranchus

Fig. 186. Hind legs of various tetrapods.
F. femur; FI. fibula; T. tibia. (Modified from Evans.)

(3i6)

Fig. 187. R. temporaria dissected from the back.

add. adductor; anc. anconeus ('triceps'); c. calcar; c.sacr. coccygeo-sacralis; cocc.il. coc-
cygeo-iliacus ; cue. cucullaris ; delt. deltoid ; dep. mand. depressor mandibulae ; dors.se. dorsalis
scapulae; ext.obl. obliquus externus abdominis; fasc. dors, dorsal fascia; fl.hr. flexor brevis;
gastr. gastrocnemius; glut, gluteus; il. ilium; il.ext. iliacus externus; il.fib. ilio-fibularis;
lat.dors. latissimus dorsi; I. dors, longissimus dorsi; n. nostril; peron. peroneus; pir. piri-
formis; rhomb, rhomboideus; semi.m. semimembranosus; semi.t. semitendinosus; t.Ach.
tendo Achillis; t.f.lat. tensor fasciae latae; tib.ant. tibialis anterior; tr. transversus abdo-
minis; tymp. tympanum. (Partly after Gaupp.)

xii. io AMPHIBIAN LIMBS 317

carpals, and 7 or 8 digits. In the amphibian *Eryops most of the digits
radiate from the radius, in later forms mostly from the ulna. Moreover,
in the hand of *Eryops there seem to have been six digits and it is
usually stated that the first of these is a pre-pollex 'not comparable
with the pollex of higher forms'.

The effect of this system is to provide a lever that can be held
firmly against the ground while it is moved by the muscles running
from the girdles to the humerus or femur. In addition the lever is
itself extensible by means of its own muscles. Whatever may have
been their origin in fishes these muscles in tetrapods work in such a
way as to bend each segment up and down. The shoulder and thigh
joints usually allow movement in several planes, both towards and
away from the midline (adduction and abduction), and forwards and
backwards (protraction and retraction). As we have seen, the animal
balances at these joints by muscles arranged round them. Movements
of rotation are also possible at these, and sometimes at other joints,
the distal bone turning about its own axis on the proximal one. Such
movements may be very important for the proper placing of the limbs
in walking. Pronation is the rotation of the radius about the ulnar
bone, so that the manus is directed caudally, supination being the
opposite movement. The terms flexion and extension are convenient
at certain joints (e.g. the elbow), but have no consistent meaning with
reference to the main axes of the body.

The limbs of the earlier amphibians were ponderous affairs, with
large bones and widely expanded hands and feet (Figs. 181 and 182).
It is not certain exactly how they were used ; probably they were held
out sideways, giving a wide base on which the somewhat precarious
balance was maintained, the body being often slumped on to the
ground. In modern urodeles the limbs retain the full pattern of parts,
but with imperfect ossification, as would be expected since they carry
little weight.

In frogs, specialized for jumping, the radius and ulna are united and
the carpals are reduced in number. There are only four true digits, the
first digit (thumb or pollex) being reduced. There is, however, a small
extra ossification, the pre-pollex, which becomes well developed as a
copulatory organ in the male and may be compared with a similar
digit found in some stegocephalians. It is to be expected that in a
system of repeated parts, such as a tctrapod limb, multiplications and
reductions will be common. It can be imagined that they can be
produced by changes in the rhythm of morphogenetic processes, and
it is surprising that there is such constancy in number of digits.

3i8

AMPHIBIA

The hind legs of frogs are long, giving a good leverage in jumping.
The tibia and fibula are united and the proximal row of tarsals is
reduced to two, greatly elongated and known as the tibiale (astragalus
or talus) and fibulare (calcaneum). The distal tarsals are reduced to a
total of three, bearing five 'true' digits and an extra one, the calcar or
prehallux.

semL m

Fig. 188. Deeper dissection of muscles of back
of frog.

i.lr. inter-transversarii; ur. urostyle; v. vertebra; other
letters as Fig. 187. (Partly after Gaupp.)

1 1 . The back and belly muscles of Amphibia

With the change in the method of locomotion the muscular system
has become greatly modified from that found in fishes. In urodeles,
which still use the old method and hence may be said to swim on land,
the dorsal musculature is well developed (Fig. 189), but in anurans the
dorsal portions of the myotomes, the epaxial musculature, no longer
have to produce the locomotory effect by lateral flexion. They remain
in frogs only as muscles that bend the body dorsally, serving to brace
the vertebral column on the sacrum (Figs. 187 and 188). Short
muscles run between the vertebrae, and dorsal to these is a continuous
sheet of longitudinally arranged fibres, the longissimus dorsi muscle,
running from head to sacral vertebra and urostyle. This muscle,

XII. II

MUSCLES OF THE BACK

3i9

though forming a continuous band, is crossed by a tendinous inter-
section, showing its segmental origin. At the hind end the coccygeo-
sacralis and coccygeo-iliacus muscles brace the urostyle on the pelvic
girdle.

The pectoral girdle is attached to the axial skeleton by a series of
muscles. Rhomboid and levator scapulae muscles run from the supra-
scapula to the vertebrae and skull. The cucullaris muscle corresponds

rect.

Fig. 189. Muscles of larval Amby stoma. A, b, and c show successive layers.

ep. epaxial muscles; ext.o. external oblique; h. horizontal septum; hyp. hypobranchial

muscles; int.o. internal oblique; my. myocomma; rect. rectus abdominis; tr. transversus

abdominis. (From Ihle, after Maurer.)

to the mammalian sternomastoid, running from the skull to the
suprascapula; it is derived from lateral plate musculature and in-
nervated by the vagus. The naming of these muscles of the scapula,
and indeed all amphibian muscles, meets the difficulty that many of
the bundles of fibres are similar in their general course to muscles
found in mammals and yet differ sufficiently to raise serious doubts
about the wisdom of using the mammalian names. The similarity of
arrangement of the limb muscles is so striking throughout the tetra-
pods that there is probably no harm in keeping to the well-established
system of names, but we know so little of the hereditary or mechanical

(32°)

svbmax,
om
sub.hy.

ext. obi.

Fig. 190. R. temporaria dissected from the ventral surface.

add. aductor magnus; add. long, adductor longus ; anc. anconeus; br.r brachio-radialis ;
cl. clavicle ; co. coracoid ; cr. cruralis ; delt. deltoid ; ep. episternum ; ext. obi. obliquus externus
abdominis ; fix. rad. flexor carpi radialis ; fl.c.uln. flexor carpi ulnaris ; gastr. gastrocnemius ;
grac. ma}, and min. gracilis major and minor; il.int. iliacus internus; o.h. omohyoid; om.
omosternum; pect. pectoralis; r.s. rectus sheath; red. rectus abdominis; sart. sartorius;
st.h. sterno-hyoid; submax. submaxillary; sub.hy. subhyoid; t.Ach. tendo Achillis; t.f.lat.
tensor fasciae latae; tars. a. and tars. p. tarsalis anterior and posterior; tib.ant.br. and long.
tibialis anterior brevis and longus; tr. transversus abdominis; .yj. xiphisternum.
(Partly after Gaupp.)

XII. II

VENTRAL MUSCLES

321

factors that control the arrangement of muscle-fibres into 'muscles'
that discussion of homologies is difficult.

The hypaxial musculature, formed from the more ventral portions
of the myotomes, is more developed than in fishes and differentiated
into several parts, for the purpose of slinging the viscera, which of
course need support in air in a way that is unnecessary in water.

sub. max.

dep. mand.

d. rorrad
deU.

h..

Fig. 191. Dissection of muscles of frog from ventral surface.

cor.br. coraco-brachialis; cor.rad. coraco-radialis; dep. mand. depressor mandibulae; h. head of

humerus; s. sternum; other letters as Fig. 190. (Partly after Gaupp.)

These muscles are differentiated into layers whose fibres run in
different directions. The plan found, with modifications, in all
tetrapods is seen in amphibian larvae and includes four sets of fibres.
The external obliques run caudally and ventrally; inside this
layer is the internal oblique, running in the opposite direction, and
within this again the transversus abdominis running approximately
dorso-ventrally (Fig. 189). The rectus abdominis consists of fibres in
the midline running antero-posteriorly.

In the adult frog three of these sets of fibres can be recognized. In
the mid-ventral region (Fig. 191) are the longitudinally arranged
fibres of the rectus abdominis, making a sling between the sternum
and the pubis. These fibres are interrupted at intervals by transverse
fibrous tendinous inscriptions, giving an appearance of segmentation.
In the mid-ventral line is the tendinous linea alba. The sling formed

322

AMPHIBIA

by the rectus abdominis is supported laterally by thin sheets of
muscle-fibres running up to the vertebral column, the obliquus exter-
nus and transversus abdominis (Fig. 191).

In the anterior region the hypaxial muscles have become restricted
to the throat, where they form the hyoid musculature, which by raising

Fig. 192. a. Lateral surface of the fin of Neoceratodus, showing the abductor

muscle-bundles, b. Section through the fin in the transverse plane, showing the

arrangement of the muscle-bundles as abductors and adductors.

ab. abductor muscles; ad, adductor muscles; g. pectoral girdle; h. horny fin rays;

r. radials. (From Ihle, after Braus.)

and lowering the floor of the mouth is the main agent of breathing.
The submaxillary muscle runs transversely between the rami of
the jaw. Deep to this lie other muscles, including the sternohyoid,
close to the midline, which is a forward continuation of the rectus
abdominis.

12. The limb muscles of Amphibia

The muscles of the limbs were presumably derived from the radial
muscles that moved the fins of fishes. These are formed from the
myotomes and they are mainly arranged so as to raise and lower the
fin (Fig. 192). In modern amphibia the limb musculature is still partly
formed from myotomes (Griffiths, 1959). The segmental origin of the

xii. 12 LIMB MUSCLES 323

limbs is also shown by the fact that they are innervated by branches
of the spinal nerves of several segments (2 for the fore-limb, 4 for the
hind-limb in the frog). Presumably the original arrangement was such
as to move the limbs in association with the waves of contraction
passing down the body. In modern urodeles the limb is brought
forward and its joints flexed as the epaxial muscles at the level of its
front end contract, and then passes back and extends as the wave of
contraction moves past. This may have been the primitive movement,
making the limb more useful as a lever during the early attempts to
'swim on land' (Fig. 176).

The muscles of the limbs of tetrapods are presumably derived from
those that raise and lower the fins of fishes, modified, as we have seen,
to brace the limbs and move them, allowing standing and walking.
The muscles that run from the girdles to the humerus and femur are
therefore able to draw the leg forward and backward, as well as to
raise and lower it in the transverse plane. The actions of the various
bundles are of course not confined to a single plane: all the muscles
running from the back to the humerus can raise (abduct) the upper
limb, but the more anterior members also protract, the more posterior
retract it. Similarly there is a ventral series whose anterior members
work with the anterior dorsal muscles as protractors, although they
antagonize the action of raising the whole limb. Moreover, many of the
muscles have a rotating action on the humerus and femur. It is, how-
ever, possible to consider the muscles of the arm and leg in two great
groups; first a more anterior and ventral ('ventro-lateral') set serving
to draw the limb mainly forward and towards the midline (protraction
and adduction) and to flex its more distal joints, second a more
posterior, dorsal ('dorso-medial') mass serving mainly to draw the
limb backwards and away from the body (retraction and abduction)
and to extend its joints.

In the fore-limb the proximal members of the ventral group make a
sheet of fibres running transversely to the main body axis and attached
to the sternum and hypaxial muscles at one end and to the humerus at
the other (Fig. 190). Within this sheet can be recognized the del-
toideus, pectoralis, coraco-radialis, and coraco-brachialis muscles. In
the limb itself this group is continued, there being, roughly speaking,
a set of muscles in each segment that serves to flex it on the next.
Thus the brachio-radialis flexes the elbow joint and in the forearm
the flexor carpi radialis and flexor carpi ulnaris flex the wrist. The
flexor digitorum longus muscle arises from the medial epicondyle of
the humerus and is inserted by tendons to the carpus and terminal

324 AMPHIBIA xn. 12-

phalanges. Flexor digitorum brevis muscles arise from this tendon
for insertion on the digits.

Of the dorsal muscle mass (Fig. 187) the latissimus dorsi and
dorsalis scapulae are the most proximal, running from the middle of
the back to the humerus and serving to abduct and draw back the
whole limb. The triceps (anconeus) serves to extend the elbow; in
the forearm are extensor carpi ulnaris and radialis and extensors for
the fingers.

According to this plan protractor (flexor) muscles lie mainly an-
terior to retractors (extensors), corresponding to the ancient move-
ment by which the limb was drawn first forward then back as a swim-
ming wave passed down the body. In all tetrapods flexor muscles are
in general innervated by spinal roots anterior to those for the exten-
sors. The locomotory movements of the limbs therefore still show the
passage of an excitation wave backwards along the spinal cord, a relic
of the swimming rhythm of fishes. However, the changes that have
taken place in the relative positions of the parts of the limbs make it
difficult to follow out this simple pattern in detail. It must also con-
tinually be remembered that many muscles produce rotation as well
as movement in the main planes of the body.

In the hind limb, muscles of the same two general types can be
recognized, namely anterior muscles, which draw the limb forward
and flex and adduct its joints, and posterior ones, which draw it back
and extend and abduct. The specialization of the main muscle masses
has gone much farther, however, so that more individual muscles are
found, especially round the hip joint, each serving to move the limb
in a special way.

In the thigh (Figs. 187 and 190) the muscles of the anterior group,
lying on the ventral surface, are the pectineus and the adductors,
running from the pelvic girdle to the femur and thus serving to move
the whole limb inwards (adduction). The sartorius, biceps, semi-
membranosus, and semitendinosus are two-joint muscles mainly pro-
ducing flexion at the knee as well as at the hip.

The more posterior and dorsal group of muscles includes the
gluteus and tensor fascia lata from girdle to femur, extending the
thigh joint, and the very large cruralis (including the rectus femoris
and triceps femoris) running from girdle and femur to tibia. This is
the main extensor of the knee, being helped by gracilis and semi-
membranosus. This extension is obviously an important part of the
jumping movement of the frog.

In the shank the arrangement of the flexors and extensors into the

Y
ppa

/><!

ac.

St.

p rose.

xii. 13 LIMB MUSCLES 325

anterior and posterior groups is much modified. The more con-
spicuous muscles are the tibialis anterior and peroneus running from
the femur to the tarsus so as to flex the ankle joint. Long and short
flexors move the toes, as in the fore-limb. At the back of the tibio-
fibula the gastrocnemius (plantaris longus) runs from the femur to
be attached by the tendo Achillis to the tarsus. Its main action is to
extend the ankle in the movements of jumping and swimming. Tibialis
posterior runs from the tibia
to the tarsus. Within the foot
there is an elaborate system of n — i~~P m -

small muscles for bending and
stretching the toes and abduct-
ing them away from each other,
so as to expand the web for
swimming.

The whole system is de-
signed to produce the charac-
teristic sudden simultaneous
extension movement of all the
joints of both hind limbs, by
which the frog moves both in
water and on land. The hind
limbs can also be used for
alternate walking movements,
especially in toads (Fig. 177).

13.

ttPi

Fig. 193. Diagram of skull bones and other
structures, a, an osteolepid ; B, astegocephalian.

Letters for this and Fig. 194: ac. auditory capsule;
ex. extrascapular; jr. frontal; hm. hyomandibula ;
it. intertemporal; j. jugal; /. lachrimal; na. nasal;
?nx. maxilla; p. pineal; pa. parietal; pi. pituitary;
pm. pre-maxilla; po. post-orbital; pof. post-frontal;
ppa. post-parietal; prf. pre-frontal; p.rost. post-
rostrals; qj. quadratojugal; sq. squamosal; st. stapes;
sut. supratemporal; t. tabular.
(After Westoll.)

The skull of Stenoce-
phalia

The skull of the Devonian
and Carboniferous amphibia

was essentially like that of the osteolepid fishes in the arrangement of
the bones, but the proportions had been altered so that the pre-optic
region was relatively large and the more posterior 'table' of the skull
short (Fig. 193).

The nasals and frontals, which were small in crossopterygians,
were quite long in stegocephalians, whereas the parietals were shorter
and the post-parietals absent altogether in the later forms. The differ-
ence is so marked that for a long time people were deceived in identifi-
cation of the bones and it was said that the pineal opening lay between
the frontal bones in fishes but between the parietal bones in tetrapods.
The bones identified as 'frontal' in the fish types were, of course,

326

AMPHIBIA

xii. 13

parietals, whereas the 'parietals' were the post parietals, which have
gone completely from most amphibians, though still present in the
earliest Devonian forms (Fig. 194). This is an excellent example of how
study of changes of proportion can clear up morphological difficulties.
The opercular apparatus covering the gills was lost early in
amphibian evolution; perhaps the reduction of the whole posterior
part of the head was effected by a single morphogenetic change. In

ppa. "— —

Osteo/epis

F/p/ftOStCLJC

Ichthyostega

sub

Palaeogurinus RomerJa Dimetrodon

(Cotylosaur) (Pelycosaur)

Fig. 194. Skulls of a crossopterygian and various early tetrapods to show the
shortening of the posterior region. Lettering as Fig. 193. (After Westoll.)

modern amphibia the skull is much flattened and its ossification
reduced, so that large spaces are left; in the earlier forms, however,
the skull was of the more usual domed shape and the roof and jaws
were covered by a complete set of dermal bones. Presumably the loss
of bone was another development producing a reduction of weight
advantageous to a terrestrial animal.

Lateral line organs are present in aquatic amphibians and their
position is marked on the bones of the fossil skulls by rows of pits.
By using these lines as reference marks it is possible to compare the

xii. i 3 STEGOCEPHALIAN SKULL 327

pattern of the bones on osteolepid and early amphibian skulls and to
confirm the remarkable similarity. The main new development found
in the skull of early amphibians was correlated with the modification
of the Eustachian tube in connexion with the sense of hearing, and
the need for a sensitive resonator to pick up the air vibrations. Already
in the earliest amphibians the opercular coverings of the gills were
lost (there was a small pre-opercular bone in *Ichthyostega) and the
spiracular opening thus uncovered acquired a tympanic membrane.
The hyomandibular cartilage, no longer concerned (if it ever had
been) with supporting the jaw, was modified to form the columella
auris, serving to carry vibrations across to the inner ear. At first,
however, there was no trace of the fenestra ovalis, the hole in the
auditory capsule into which the columella fits in the frog. In modern
urodeles the whole ear apparatus is much modified, there being no
tympanum. Instead the columella is fused to the squamosal and the
ear thus receives its vibrations from the ground.

Other small changes in the skull in passing from the fish to the
amphibian stage include the increase in size of the lachrymal bone,
which also came to have a hole to carry the tear duct, draining the
orbit. A series of small bones surrounds the orbit in early amphibians,
as in fishes; large squamosals and quadrat ojugals support the quad-
rate. At the back of the skull these stegocephalians possessed various of
the small bones that are found in fishes but not in modern amphibians,
the supratemporal and intertemporal, post-parietal (much smaller
than in crossopterygians) and tabulars. In fact there are numerous
small bones, arranged in a pattern clearly recalling that of the fish
ancestor, but showing some reductions and less variation than in those
very variable fish skulls. This simplification (which was later carried
farther), together with some changes in the shape, are the chief trans-
formations that have converted the fish skull into the amphibian
skull.

The palate of the early amphibians also resembled that of crosso-
pterygians, showing a complete plate made of vomer, palatines,
pterygoids, and ecto-pterygoids. These bones, as well as the pre-
maxillae and maxillae, often carried folded teeth (hence 'labyrin-
thodonts'), with a pit for a replacing tooth beside each one, an
arrangement similar to that of their fish ancestors (p. 270). The
internal nostril opened far forward, through the palate. The lower
jaw was covered by a number of dermal bones (Fig. 208), but the
actual jaw articulation was made between cartilage bones, the upper
quadrate, and the lower articular.

328

AMPHIBIA

xii. 14

14. The skull of modern Amphibia

Modern amphibia share several cranial features that distinguish
them from typical labyrinthodonts. The number, extent, and thick-
ness of the dermal elements are greatly reduced so that the otic

b p.

Fig. 195. Skull of the frog. a. Ventral view. b. Side view.

ac. anterior cornu of hyoid ; art. articular ; as. angulosplenial ; col. columella auris ; d. dentary ;
ex. exoccipital ; fp. fronto-parietal; m. maxilla; m.m. mento-Meckelian; n. nostril; na. nasal;
pa. palatine; par. parasphenoid; pc. posterior cornu of hyoid; pm. premaxilla; pro. pro-otic;
pt. pterygoid; q. quadrate; qj. quadrato-jugal; se. sphenethmoid; sq. squamosal; v. vomer;
//, IX, and A', nerve foramina. (After Marshall, The Frog, Macmillan.)

capsules are generally exposed. The orbits and interpterygoid vacui-
ties are large, the mandibular ramus is short and the skull as a whole
much flattened. The occiput is shortened so that the hypoglossal nerve
emerges behind the skull and (with the few exceptions noted below)
the parietal foramen has been lost.

The skull of the frog (Fig. 1 95) shows great reduction and specializa-
tion from the early amphibian type. It may be considered as consisting
of a series of cartilaginous boxes or capsules, in whose walls some
ossifications occur, partly covered by dermal bones. The cartilaginous

xii. 14

MODERN AMPHIBIAN SKULLS

329

o.F P { ar F-

cpt. %■ o.pt, cp- ps.^v. m

apt. c.M.

o.c I c - c - SALAMANDER

bc.p.

ICHTHYOPHIS

Fig. 196. Skulls of amphibians.

a., articular; be, basicranial fenestra; bc.p., posterior basicranial fenestra; c.c, carotid canal;
<-..V., Meckel's cartilage; c.p. coronoid process; cpt. pterygoid cartilage; c.r. process of
internasal plate; d. dentary; e.o. exoccipital;/. frontal ;fen.ol. olfactory fenestra; in. internal
naris;_/. jugal; m. maxillary; m.M. mento-Meckelian; ;;. nasal; o.c. occipital condyle;
o.f. optic foramen; o.p. occipito-petrosal; ope. operculum; o.pt. pterygoid bone; o.s. orbito-
sphenoid; p. a. pre-articular; par. parietal; p.f. prefrontal; p. I. palatine; p.m. premaxilla;
po.f. postfrontal (enclosing orbit); p.q. palato-quadrate; pr.ba. basal process; p.s. para-
sphenoid; p.v. prevoma; q. quadrate bone; sq. squamosal; st. stapes; /. tentacular groove;

v. vomer.

boxes, well seen in a tadpole's skull, are the central neurocranium
around the brain, and the olfactory and auditory capsules. Ossifications
occur especially at the points of compression stress, namely, around
the foramen magnum (the exoccipitals), where the auditory capsule
joins the cranium (the pro-otic), and at the base of the nasal capsules
(the mesethmoid). The paired occipital condyles are found only in

33° AMPHIBIA xn. 14

modern amphibia, and are formed by the failure of the basioccipital
to become ossified. Paired occipital condyles have also arisen, inde-
pendently, in the mammal-like reptiles.

The dermal bones covering the roof of the skull are the nasals and
frontoparietals, while on the floor is the large dagger bone, the
parasphenoid, and a small tooth-bearing vomer. The remains of the
cartilaginous palato-pterygo-quadrate bar can be recognized as a rod,
covered in front by premaxillae and maxillae, and dividing behind
into an otic process fixing it to the skull (autostylic) and a cartilaginous
quadrate region articulating with the lower jaw. This region is covered
by the pterygoid ventrally, the quadrato-jugal laterally, and the
squamosal dorsally. The palatines are membrane bones forming the
anterior wall of the orbit. The upper jaw is thus supported by struts
formed from the nasals and palatines in front and the squamosal and
pterygoid behind, an arrangement that gives a large mouth for res-
piration and eating insects, combined with the advantages of strength,
mobility of the lower jaw, and lightness in weight.

The lower jaw consists of Meckel's cartilage, covered on its outer
surface by a dentary and on its inner by an angulo-splenial bone.
The anterior tips of the cartilages ossify as the mento-Meckelian bones .

The visceral arches are well formed in the tadpole but are much
modified in the adult frog. In the tadpole the skeleton of the hyoid
arch consists of a large pair of ceratohyals attached to a basal hypo-
hyal. As a result of subsequent metamorphosis the ceratohyals later
form the long anterior cornu of the hyoid, attached to the pro-otic
bone. The body of the hyoid is a plate lying in the floor of the mouth
and formed from the hypohyal and from the hypobranchial plate at
the base of the remaining arches. The posterior cornua support the
floor of the mouth and the whole apparatus assists in respiration. The
sixth and seventh of the series of branchial arches give rise respec-
tively to the arytenoid and cricoid cartilages of the larynx.

The lateral plate muscles of the branchial arches are well developed
only as the muscles of the jaws. Certain muscles of the scapula (the
cucullaris (p. 319) and interscapularis) are innervated from the vagus
and recall the sternomastoid and other muscles innervated by the
spinal accessory nerve in mammals.

The muscles of the hyoid arch, innervated by the facial nerves,
remain mainly as the depressor mandibulae (Fig. 197) running from
the back to the angle of the jaw and serving to lower the floor of the
mouth. The jaw-closing muscles, m.m. adductor mandibulae, belong
to the mandibular segment and are innervated by the trigeminus.

xii. 14 EVOLUTION OF THE SKULL 331

They run from the hind end of the jaw to the surface of the skull and
squamosal.

The skull and jaws of the frog thus constitute a protection for the
brain and special sense-organs, a feeding apparatus, and a means of
respiration. The heavy protection afforded by the dermal bones of
fishes and early amphibians has been largely dispensed with, probably
for lightness. The front part of the skull, concerned with the nose,
eyes, and brain, has become increased in size and the hind part,
originally concerned with the gills and pharynx, greatly reduced.

dep.mand.

Fa se. dors,
iat. dors.

cor rad
FL. c uin.

Fig. 197. Muscles of head and neck of frog dissected from the side.
add. adductor mandibulae. Other letters as in Figs. 187 and 191. (Partly after Gaupp.)

These changes, carried to extremes in frogs, have been in progress
throughout the evolution of amphibia. It is not difficult to imagine
that they have been the result of rather simple genetic changes, affect-
ing the relative growth of various parts of the skull. We are still far
from the knowledge necessary to say exactly what developmental
changes have occurred, but we know enough to imagine how selection
through millions of years has changed the quantities of certain sub-
stances so as to produce gradually less bony and shorter heads, such
as enabled their possessors to maintain sufficient mobility to hold a
place in a world peopled by the reptiles and other still more active
descendants of the early amphibians.

The preceding account, particularly with regard to the osteology,
should not be regarded as diagnostic of all anurans. Bufonid skulls
are completely devoid of teeth but they possess a supratemporal bone,
which fuses with the squamosal and roofs the otic capsule. Hylids
frequently develop secondary dermal ossifications to form expanded
helmets; this trend also occurs in leptodactylids (e.g. Calyptocephalus),
where the skull may be so completely roofed and sculptured as
to simulate the condition of the extinct branchiosaurs. Pseudoteeth

332 AMPHIBIA xn. 14-

(serrations of the jaw elements) frequently occur on the dentary and
pre-articular (e.g. Amphodus) but the only modern form to possess
true teeth on the lower jaw is Amphignathodon. No recent frog retains
the large parietal foramen so typical of the fossil amphibia but some
leptodactylids and the aquatic xenopids have a small canal perforating
the fronto-parietal, through which runs a fibro-nervous tract from the
pineal organ to the habenular ganglion (Griffiths, 1954). The anuran
skull is always easily distinguished from those of all other Amphibia
by the fact that the frontals are fused with the parietals.

Urodele skulls are, in some respects, less specialized than those of
Anura. The frontals and the parietals remain discrete and in certain
species both lacrimals and prefrontals are present. In other respects
they are clearly more degenerate (or paedomorphic ?). No urodele has
either a jugal or quadrato-jugal (except Tylotriton) and in perenni-
branchs even the maxillaries and nasals are lost. Urodeles are further
distinguished from frogs (but not from caecilians) by the great size
of the prevomers (each consisting really of a prevomer+ palatine) and
by the possession of a tooth-bearing coronoid, as well as a dentary
and a prearticular.

The apodan skull is a much more rigid structure than that of either
of the above subclasses and, at first sight, approaches more closely to
the ancestral pattern. The number of bones present, however, is no
greater than in any of the other modern groups. The overall compact-
ness is effected particularly by the expansion of the nasals and of the
marginal elements of the upper jaw and is probably correlated with the
burrowing habits of the group. Lower as well as upper jaws carry
teeth and a toothed coronoid is present in the mandible.

15. Respiration in Amphibia

The new problems presented by life on land have led to the produc-
tion of very varied means of respiration among amphibia. In a ter-
restrial habitat oxygen is available in plenty; the difficulty is evidently
to arrange for a regular interchange of air in contact with adequately
moistened surfaces. The interchange is provided for in most cases
by modifications of the apparatus used in fishes, but pumping air
presents new problems and it seems that these are not easily solved,
since in many amphibians the skin is used as an accessory respiratory
mechanism. The retention of moisture becomes more difficult as the
ventilation becomes efficient; probably for this reason air is often
only transferred to the lungs after it has remained for some time in the
mouth. We see again that the new way of life, in a medium remote

xii. 1 6 RESPIRATION 333

from water, makes it necessary to possess more complicated methods
of self-maintenance.

16. Respiration in the frog

The lungs of the frog are paired sacs, opening to a short laryngeal
chamber, which communicates with the pharynx by a median aper-
ture, the glottis. The glottis and laryngeal chamber are supported by
the arytenoid and cricoid cartilages. The arytenoids guard the open-
ing of the glottis and are moved by special muscles. During breathing
the mouth is kept tightly closed, the lips being so arranged as to make
an air-tight junction. Air is sucked in through the nostrils by lowering
the floor of the mouth by means of the hypoglossal musculature, and
can then either be breathed out again or forced into the lungs by
raising the floor. The external nares are closed by a special pad on the
anterior angle of the lower jaw, supported by the mento-Meckelian
bones. This pad is thrust upwards and pushes the premaxillaries
apart, so altering the position of the nasal cartilage that the nostrils
are closed. This is a special mechanism, found only among anurans.
In urodeles the nostrils are closed by valves provided with smooth
muscles. Such valves are present in the frog but are said to be func-
tionless.

The movements of the floor of the pharynx are not continuously of
the same amplitude. After a period of relatively slight movements the
nostrils are kept closed while the throat is lowered. Air is thus drawn
from the lungs and then again returned to them once or twice before
the nostrils are reopened. The whole procedure presumably ensures
the maximum gaseous interchange for the minimum water-loss.

This method of taking in air is clearly derived from the movements
of the floor of the mouth of fishes, by which water is passed over the
gills. In amphibian larvae water is pumped in this way and there is
direct continuity between the mechanism of larva and adult. The
basic rhythmic mechanism, centred on the nerve-cells of the medulla
oblongata, is no doubt the same throughout, but the anurans have
improved upon it by the addition of special features, requiring intri-
cate coordination of the muscles of the larynx and the apparatus for
closing the nostrils.

The skin is very vascular, and especially so in the buccal cavity. It
plays a large part in respiration, actually serving to remove more
carbon dioxide than do the lungs. There is, however, little power to
vary the amount of exchange through the skin, which is therefore
constant throughout the year. There is considerable regulation of the

334 AMPHIBIA xh. 16-

exchange in the lungs. The rate of breathing depends, as in mammals,
on the effect of the carbon dioxide tension of the blood on a respira-
tory centre in the medulla. There is also a vasomotor control of the
blood-supply to the lungs and, through the vagus nerve, of the state
of contraction of the latter. By such means the rate of respiratory
exchange is greatly increased during the breeding season, and made
to vary with the activity of the animal.

17. Respiratory adaptations in various amphibians

The skin and the lungs show many variations according to the
habitat of the species, special devices being adopted to enable the
animals to live in particular environments. The lungs vary from the well
vascularized sacs with a highly folded surface found in the frogs,
and especially in the drier-skinned toads, to small simple sacs in some
stream-living amphibia. The lung will serve to lift the animal in the
water; for this reason it is reduced in the frog Ascaphus, which lives in
mountain streams in the eastern U.S.A. In newts this hydrostatic
function of the lungs is predominant and the inner surface is often
quite simple. The lung is entirely lost in stream-living salamanders,
such as the European alpine S. atra. The coldness of the water reduces
activity and lowers the need for respiratory exchange to a level at
which it can be fully met by the skin. The skin shows increased vascu-
larity in these forms with reduced lungs, capillaries reaching nearly
to the outermost layers of the epidermis. In the African frog Astylo-
sternus, in which the lungs are vestigial, the male develops vascular
papillae on the waist and thighs during the breeding season.

Gills are present in amphibian larvae, and also in certain adult
urodeles that may be considered as larvae that have failed to undergo
metamorphosis (p. 364). The gills are extensions of the branchial
arches, and carry branched villi, richly supplied with blood. Where
the main trunk is long the gill projects and is 'external', whereas in
other cases, as in the later frog tadpole, the filaments are directly
attached to the arches and are called 'internal'. There are no profound
differences between the two types.

18. Vocal apparatus

Sound is produced as a protective (fear) response and by the male
frog as a call to attract the female. Both sexes have vocal organs, but
those of the female are much the smaller. The noise is produced by
the vibration of the elastic edges of a pair of folds of epithelium of the
laryngeal chamber, the vocal cords. Air is passed backwards and

xii. iQ

(335)

Uroddd, larva

FlG. 198. Diagrams illustrating development and fate of aortic arches in Amphibia,

left-side view completed. Vessels carrying most arterial blood white, most venous

blood black, and mixed blood stippled.

a 1-6 , Primary arterial arches; ca. conus arteriosus; cb. carotid gland; cc. common carotid;
da. median dorsal aorta; db. ductus Botalli; dc. left ductus Cuvieri; ec. external carotid;
eg. blood-supply to external gill; ic. internal carotid; la. left auricle; Ida. lateral dorsal
aorta (d. obliterated part, ductus caroticus); Ig. lung; oph. ophthalmic; or. orbital; pa.
pulmonary artery; pea. pulmo-cutaneous arch; pv. pulmonary vein; s. closed spiracular slit;
sa. systemic arch; sv. sinus venosus; tra. truncus arteriosus (ventral aorta); v. ventricle;
vci, vena cava inferior. (From Goodrich.)

forwards between the lungs and a large pair of sacs (or a single median
sac), the vocal pouches, formed below the mouth. These also serve as
resonators, and are developed only in the male.

19. Circulatory system of Amphibia

The venous and arterial systems arc less fully separated in Am-
phibia than in lung-fishes. The auricles are completely divided by an
inter-auricular septum, venous blood returning to the right, arterial
to the left auricle. There is only a single ventricle, but this is provided
with spongy projections of its wall, which may prevent the mixing of
the blood. The ventral aorta (conus arteriosus), springs from the

336 AMPHIBIA xn. 19

right side of the ventricle and may thus receive first the venous blood.
The conus arteriosus has transverse and longitudinal valves.

The ventral aorta is very short and the arches much modified in the
adult (Fig. 198). Of the original six that can be recognized the first

Ophth

A a . abdom

Ailiaca comm
A.epiy.-ves

A. ischiadica

Fig. 199. Diagram to show the chief arteries and
their anastomoses in the frog. (After Gaupp.)

two disappear, the third on each side gives rise to the carotid artery,
the fourth remains complete and forms the systemic arch. The fifth
remains also in some urodeles, but disappears in anurans. The sixth
arch becomes the pulmonary artery and loses its connexion with the
dorsal aorta: special 'cutaneous arteries' carry de-oxygenated blood
from this arch to the skin (Fig. 199). These pulmonary arches prob-
ably offer a lesser resistance than do the systemic and carotid ones;
the pressure in the latter is said to be increased by a special network,
the 'carotid gland', though it may well be that this organ is a receptor,

xii. iq CIRCULATION 337

connected with regulation of the blood-pressure. However, it is
claimed that the first blood leaving as the ventricle contracts flows to
the lungs. In anurans this separation may be further assisted by an
arrangement such that the pulmonary arteries join at their base and

V pulmon dext

Vjug int
Vjug ext
v subscap
Vanonyma
— Vsubc/avia
V. brachlabs
V. cutan. magna

V cava ant

PuLmo dext.

V bulb cord, post

V cava post

V dorso-lumb.
V. abdomen
Vjacobsonn
V oviduct-
Oviduct
V dxaca communis

V 'renal reveh

V hepat. (revehens)

Intestlnum

V porta e hepat

Ovarium

V.ovarica

R.abdommaUs (VfemorJ

V dica ext

V ilica transversa

V ischiadica

V FemoraliS.

Fig. 200. Diagram to show the chief veins of the frog. (After

Gaupp.) The r. abdominalis is often called the pelvic and the

v. iliaca communis the renal portal vein.

open to the dorsal part of the truncus arteriosus (cavu'm pulmo-
cutaneum), which is partly separated from the more ventral cavum
aorticum, leading to the carotid and aortic arches. The classical view
of this system is that as the pressure rises the truncus contracts and
the spiral valve moves in such a way as to force all the blood that
leaves the ventricle during the later part of its contraction into the
ventral portion and hence to the systemic and carotid arches. In this
way a separation of blood from the right and left auricles would be
achieved. The view that the heart allows such a separation has, how-
ever, been challenged on the basis of experiments made by injection

338 AMPHIBIA xn. 19-

of X-ray opaque material, allowing the course of the circulation to
be watched. It is stated that by this method it can be shown that
blood returning to either auricle reaches all parts of the ventricle and
that no separation occurs. Since the blood from the skin returns to
the right auricle (Fig. 200) it is not clear that a separation of the
streams would be advantageous. It may be that the undivided con-
dition of the ventricle in amphibians is a secondary development,
perhaps not present in the earlier forms such as *Eogyrimis, which
reached a larger size (Foxon, 1955). The spongy walls of the ventricle
may allow metabolic exchange since the heart is provided only with
very small coronary arteries.

The venous system (Fig. 200) is based on the same plan as that of
Dipnoi. The posterior cardinal veins are replaced early in life by a
vena cava inferior. Most of the blood from the hind limbs passes
through the renal portal system, but there is an alternative path
through pelvic veins and a median anterior abdominal vein, which
breaks into capillaries in the liver.

The blood-pressure is regulated by the extrinsic nerves of the heart,
fibres from the vagus tending to slow and from the sympathetic
nervus accelerans tending to speed the beat. The latter nerve is a
new development, there being no sympathetic innervation of the
heart in fishes (the condition in Dipnoi is unknown). The diameter
of the arteries throughout the body is also under control from sym-
pathetic vasoconstrictor and perhaps also vasodilatator nerves. The
arterioles in the web of the foot can be seen to constrict when the
medulla oblongata is stimulated. Substances extracted from the
posterior lobe of the pituitary and from the adrenal medulla also serve
to cause constriction of the arteries and perhaps also of the capillaries.

There is therefore a complex mechanism for ensuring that the pres-
sure of the blood is maintained and the flow directed into the part of
the body that requires it for the time being.

20. Lymphatic system of Amphibia

The transfer of substances between the cells and the blood-stream is
effected in any vertebrate by a transudation through the walls of the
capillaries into the tissue fluids. Under the pressure of the heart-beat
water and solutes leave the capillaries, passing through their walls,
while proteins remain behind. The blood passing into the venous
ends of the capillaries therefore has a high colloid osmotic pressure
and this serves to suck back fluid from the tissues. In this way a
circulation from the capillaries into the spaces around the cells is

xii. 21 BLOOD OF AMPHIBIA 339

produced. Clearly, however, it is essential for this mechanism that
the pressure of the ventricular heart-beat shall exceed the colloid
osmotic pressure of the blood. This it does by about three times in the
frog.

The lymphatic system consists of a set of spaces which, in the frog
at least, communicate with the tissue spaces around the capillaries.
Injection of gum into the lymphatic system, by increasing the colloid
osmotic pressure in the tissue spaces, prevents the back suck of fluid
into the venules and hence leads to swelling of the part injected. The
lymph spaces in the tissues join to form larger channels and great
sinuses, such as that below the loose skin of the back of the frog. The
lymph is kept circulating by the action of lymph hearts. In the frog
there are anterior and posterior pairs of these, opening into veins. The
more posterior pair lies on either side of the coccyx and can be seen if
the skin is removed. The lymphatic vessels also assist in the process
of repair. If, after injury, red cells come to lie in the tissues the lym-
phatics send out sprouts for as far as -^ mm to pick them up and
return them to the blood-stream.

21. The blood of Amphibia

The red corpuscles of amphibia are much larger than those of
mammals, reaching in the urodele Amphiuma the immense size of
yofx; they nearly always exceed 20 fi. The red cells are formed mainly
in the kidney, and are destroyed, after a life of about 100 days, by the
spleen and liver. The bone-marrow is a source of red cell formation
in Ra?ia temporaria but not, except during the breeding-season, in
R. pipiens. A process of breaking up of the red cells occurs after they
have entered the blood-stream, giving a number of enucleated frag-
ments, and this, when the part remaining with the nucleus is small,
produces a result like the extrusion of the nucleus during the develop-
ment of the red cell of mammals. In Rana only small portions of the
cytoplasm are broken off in this way, but in Batrachoseps a large
proportion of enucleated corpuscles is produced.

The haemoglobin of the frog has a lower affinity for oxygen than
that of mammals, even when both are considered at the same tempera-
ture, and in this respect is notably less efficient. Also, although the
power of the blood to combine with carbon dioxide is great, there is a
less delicate regulation of the reaction of the blood than in mammals.

The white cells of amphibia are of three types, lymphocytes, with a
large nucleus and small cytoplasm, monocytes, which are larger
phagocytic macrophages, and polymorphonuclear granulocytes.

34° AMPHIBIA xn. 21-

These last may be neutro-, eosino, or basiphil and are migratory and
phagocytic. Thus the white cell picture with which we are familiar in
mammals was evidently established a very long time ago.

There is a globular spleen near the tail of the pancreas.

The blood of frogs also contains numerous small platelets (thrombo-
cytes), which probably break down when in contact with foreign
surfaces to produce the thrombin that combines with the fibrinogen
of the blood-plasma to produce clotting.

22. Urinogenital system of Amphibia

The excretory organs of adult amphibia are always the tubules of
the mesonephros. In Rana, where there is a general shortening of
the body, these extend over only a small number of segments and the
kidneys are compact. In urodeles and the primitive frog Ascaphus
the kidneys are elongated and show some evidence of their segmental
nature. The mesonephros consists essentially of a series of tubules
leading from the nephric funnels to the Wolffian duct. In the frog the
funnels do not open into the tubules, however, but into the veins;
moreover, they form independently of the rest of the tubule. In the
adult there are some 2,000 glomeruli, from each of which a short
ciliated tube leads to the proximal convoluted tubule. There follows
a second short ciliated region, corresponding in position to the Henle's
loop of mammals, and leading to a distal convoluted tubule, which
joins the Wolffian duct.

The blood-supply of the kidney differs from that of mammals in
that blood arrives from two distinct sources; the branches of the
renal artery run mainly to the glomeruli, those of the renal portal
vein to the tubules. This corresponds to the functions now well
established for those two parts, namely that the glomerulus filters off
water and crystalloids, some of which are then reabsorbed by the
tubule. Many details of this process are not clear, however, for
instance how the urea concentration in the urine is raised many times
above that of the blood.

The frog, having a moist skin, is presumably in constant danger of
osmotic flooding with water when it is submerged, and of desiccation
when on land. The flooding is prevented by the efficient functioning
of the glomeruli; they allow the frog to excrete as much as one-third
of its weight of water per day (man i/50th). The mechanisms for
resistance to desiccation are less perfect. There is no long water
reabsorbing segment, the part of the tubule corresponding to Henle's
loop being short. There is, however, a large cloacal (allantoic) bladder

xii. 22 REPRODUCTION 341

(to be distinguished from the mesodermal bladder of fishes) from
which water can be reabsorbed. Certain desert amphibia (Chiroleptes)
conserve water by losing the glomeruli altogether. Rana cancrivora is
euryhaline and may have 2-9% of urea in the blood (Gordon 1961).

The Miillerian duct, by which eggs are carried to the exterior,
develops separately from the Wolffian system in the frog, but arises
from the latter during development in urodeles. In this, as in many
other features, the frog shows a greater degree of specialization of its
developmental processes. The ovaries are mere folds of the peri-
toneum, having no solid stroma such as is found in mammals. There
are, however, follicle cells around each egg; these presumably pro-
duce the ovarian hormones. Sections of an ovary show eggs in various
stages of development, but not all those that begin complete their
maturation; many degenerating, atretic eggs are found. Ripening of
the eggs proceeds under the influence of a hormone produced by the
anterior lobe of the pituitary. This in turn is controlled by external
environmental factors to ensure breeding in the spring. Suitable
injections of mammalian anterior pituitary extracts will ensure ripen-
ing of the ovaries and ovulation at any time of year. The 'prolans'
excreted in the urine of pregnant women have a similar effect, and
the production of ovulation in Xenopas is used as a test for the diagno-
sis of human pregnancy.

Having left the ovary the eggs find their way to the mouths of the
oviducts mainly by ciliary action of the latter. The walls of the oviduct
are glandular and secrete the albumen; they are dilated at the lower
end to form uterine sacs, in which the eggs are stored until laid.

The testes discharge directly through the mesonephros by special
ducts, the vasa efferentia, formed by outgrowths from the mesone-
phros into the gonad. This is presumably a secondary development
from the original vertebrate condition in which the sperms were
carried away by the nephrostomes. The fact that the sperms pass
through the kidney emphasizes that the amphibia have diverged at
a very early stage of the evolution of the vertebrate stock, and remain
still in many respects at a lower level of evolution than the modern
fishes, all of which have acquired separate urinary and genital ducts.
In Alytes, in many ways primitive, the sperms do not, however, pass
through the kidney!

In some frogs (R. temporaria) there is a special diverticulum, the
vesicula seminalis, leading by several small channels to the lower end
of the Wolffian duct. It contains spermatozoa during the breeding-
season and its appearance suggests a secretory activity.

342 AMPHIBIA xn. 22-

Most of the amphibia have failed to effect the complete transfer to
land life : they return each year to the water to breed. Special modifica-
tions of the reproductive system for land life are therefore not found.
Secondary sexual differences are marked in many species. In frogs
the males precede the females to the water and then attract the latter
by their vocal apparatus. The male clings to the back of the female
by means of a 'nuptial pad', developed as an extra digit, prepollex,
on the hand (p. 317). Injection of male hormones or implantation
of testis will cause this organ to develop in young female frogs.

In newts fertilization is ensured by an elaborate courtship. Sperms
are made into spermatophores by special pelvic and cloacal glands
and there are also abdominal glands, which produce a secretion attrac-
tive to the female. After a courtship ceremony the spermatophores are
picked up by the cloaca of the female and stored in a spermathecal
chamber.

23. Digestive system of Amphibia

Nearly all adult amphibia feed on invertebrates, mainly insects,
partly also worms, slugs and snails, spiders and millipedes. The larval
stages are usually omnivorous, but they may be cannibalistic, feeding
on the tadpoles of the same or other species — an interesting form of
provision for the next generation by excess productivity of the
mother. There are only minor modifications of particular species in
relation to their diet; as regards their food amphibia occupy a general-
ized or 'easy' habitat. The fact that they are not particular in choice
of diet has no doubt been part of the secret of their success.

The tongue is the characteristic organ for catching the food and is
one of the special features required for terrestrial life, being reduced
in aquatic amphibia. In Rana it is attached to the floor of the mouth
anteriorly and flicked outwards by its muscles. To keep it moist and
sticky a special inter-maxillary gland is found. From the shape of the
premaxillae it can be deduced that this gland was present in labyrin-
thodonts. The saliva contains a weak amylase and some protease. It
is suggested that these serve to release sufficient substances for tasting.
Special tracts of cilia carry the secretion from the intermaxillary
glands to the vomero-nasal organ and palatal taste-buds (Francis,
1 961).

Another feature made necessary by terrestrial life is the presence of
cilia to keep the fluids moving over the oral surfaces. These cilia are
absent in aquatic amphibia.

The teeth on the premaxillae, maxillae, and vomers are used only

xii. 23 FEEDING 343

to prevent the escape of the prey; few amphibia bite. Biting teeth
are present, however, in the adult Ceratophrys ornata, whose larvae
also have powerful jaws and are cannibalistic. The South American
tree-frog Amphignaihodon has teeth in the lower as well as the upper
jaw and presumably has redeveloped them, a remarkable case of the
reversal of evolution. Teeth are also present on the lower jaw of most
urodelcs.

dhc

Fig. 201. Transverse section of the spinal cord of a frog, showing cells in the grey
matter with their axons and dendrites spreading into the 'white' matter.

ax. axon of ventral horn cell, leaving cord in ventral root; d. dendrite of ventral horn cell;

dhc. small cells of dorsal horn; dr. dorsal root entry; m. cell body of ventral horn cell; tieur.

neuropil at periphery of spinal cord; vhc. small cell of ventral horn. (After Gaupp.)

The oesophagus is not sharply marked off from either mouth or
stomach and the latter is a simple tube. Its lining epithelium of
mucus-secreting cells is folded and simple tubular glands open at the
base of the folds. These glands, unlike those of mammals, are com-
posed of only a single type of cell, which secretes both the acid and the
pepsin found in the stomach.

The intestine is marked off from the stomach by a pyloric sphincter.
It is relatively short and dilates into a large intestine, there being a
valve interposed in the frogs, though not in all amphibia. The liver
and pancreas have the structure common to all vertebrates and pro-
duce juices of the usual type. The intestine of the omnivorous tadpole
is more coiled than that of the adult frog. The type of food taken
depends on what is available, most species of amphibia are not par-
ticular feeders. However, they can learn with only one or two trials
to avoid distasteful insects. Frogs and toads devour large numbers of
insects. If the common insects available are pests the amphibian's part
in controlling their number works to the advantage of man.

(344)

24. Nervous system of Amphibia

The organization of the nervous system of amphibia might be said
to be essentially similar to that of fishes. In both groups there are
highly developed special centres in the brain, each centre related to a

verb. 7.

n.S

n.10

n.11

Fig. 202. Ventral branches of the spinal nerves (2-1 1) of the frog. The sympathetic chain

is also shown.

g.X, vagus ganglion; int. a. intestinal artery; n.spl. splanchnic nerve; n. (2-1 1), spinal nerves;
sub. subclavier artery, sym. sympathetic chain; vert. 1, 1st vertebra. (After Gaupp.)

special receptor system. In neither group is there a dominant part,
integrating the activity of the whole, as does the cerebral cortex in
mammals.

The plan of the spinal cord is like that of fishes, but well-marked
dorsal and ventral horns are present. The large motor-cells of the cord
have dendrites that spread widely in the white matter, where their

XII. 24

BRAIN

345

synaptic connexions are made in a complicated 'neuropil' (Fig. 201).
This is a simpler arrangement than is found within the grey matter of
the mammalian curd.

n.otf.

cer.h.

cereb.

n. 9, 10,11

Fig. 203. The brain of Rana, dorsal view.

cer.h. cerebral hemisphere; cereb. cerebellum; epi. epiphysis; hth. hypothalamus; hyp. pitui-
tary gland; lam.t. lamina terminalis; olf.l. olfactory lobe; n.olf. olfactory nerve; n. 3-1 1 cranial
nerves; «. (1 and 2), spinal nerves; opt. c. optic chiasma; opt.l. optic lobe; opt.t. optic tract.
(Modified from Gaupp.)

The arrangement of the spinal nerves is much modified by the
development of the limbs. Ten spinal nerves are found but since an
embryonic first one is missing they are sometimes numbered 2-1 1 (Fig.
202). Two spinal segments contribute to the brachial and four to the
sciatic plexuses in the frog. From these plexuses fibres are distributed
to the muscles and skin of the limbs (Fig. 202).

346 AMPHIBIA xii. 24

The brain (Figs. 203 and 204) resembles that of Dipnoi very strik-
ingly. The prosencephalon is based on an inverted plan (p. 211); the
large evaginated cerebral hemispheres therefore have a thick nervous
roof as well as floor. In the frog there is only a short unpaired region
of the forebrain (diencephalon) but this is longer in urodeles. The
walls of each hemisphere may be divided into a dorsal pallium, medial
ventral septum, and latero-ventral striatum (Fig. 205). The cell bodies
lie around the ventricle in all parts of the hemisphere and there are
several layers of them. The cells are pyramidal in shape and the con-
nexions are made in the outer 'white' matter.

Nearly all parts of the hemisphere are reached by olfactory tract
fibres, the axons of the mitral cells of the olfactory bulb (Fig. 205).
In the frog there are regions at the hind end of the hemispheres that
receive forwardly directed fibres, some probably connected with tactile
and others certainly with optic impulses. There is therefore some
opportunity for the hemispheres to act as correlating centres, but we
have little information as to the functions performed in them. Their
backward projections are made by means of two large tracts, the
lateral and medial forebrain bundles, but these reach only to the
thalamus, hypothalamus, and midbrain, not back to the cord. Elec-
trical stimulation of the forebrain does not produce movements of the
animal; presumably such a crude method, though it may excite a
few neurons, cannot imitate the more subtle patterns in which they
are normally active.

Removal of the cerebral hemispheres is said to have little influence
on the normal feeding and other reactions of the frog. After this
operation the animals are said to be more sluggish, to show less
'spontaneity', and to learn less well. If the latter is true it shows a
considerable advance in the functioning of the hemispheres over the
stage reached in fishes, whose learning can certainly take place in
other parts of the brain, and is apparently little affected by removal
of the forebrain (p. 210).

Some indication of the function of the cerebral hemispheres is given
by the fact that by placing electrodes connected with a suitable am-
plifier upon them, rhythmical changes of potential can be recorded
(Fig. 206). These are most marked in the olfactory bulb and probably
propagate backwards along the hemisphere. The rhythms continue
even in a brain that has been removed from the head. They are there-
fore a sign of some intrinsic activity of the brain, rather than of re-
sponse to peripheral stimulation.

The diencephalon is interesting chiefly for the considerable number

tam.t.

Fig. 204. Two further views of the brain of Rana.
Above: ventral view. Below: lateral view. (Modified after Gaupp.)
Lettering as Fig. 203.

(34§)

Lateral

Medial

m.Fb.

olFtr

Fig. 205. Diagrams of the structure and probable cell connexions in, A, the olfactory bulb,
and b, the cerebral hemisphere of the frog.

glom. glomerulus in which fibres of olfactory nerve make contact with dendrites of mitral cells ;
gran, granule cell (cell without any axon); l.f.b. lateral forebrain bundle; m.f.b. medial forebrain
bundle; wit. mitral cell; olf.n. fibres of olfactory nerve; olf.tr. olfactory tracts; p.c. periglomerular
cell. The electrodes are shown as they would be placed for recording the potentials shown in Fig.

206. (From Gerard and Young.)

XII. 24-25 B R A I N 349

of optic tract fibres that end in its walls; other sensory projections
also reach here. In anurans, but not in urodeles, there is a partial
division into separate thalamic sensory nuclei, such as are found in
mammals, for touch, sight, and other receptor modalities.

The pineal organ shows evidence of a retina in a few amphibia;
in most it is a simple sac.

The pituitary body is well developed and the usual partes, anterior,
intermedia, nervosa, and tuberalis can be recognized, though they are
not in the same relative position as in mammals.

Fig. 206. Rhythmical changes of potential between electrodes placed on the surface
of the olfactory bulb of the frog as in Fig. 205. (After Gerard and Young.)

The midbrain is very well developed and shows many similarities to
that of fishes. The cells it contains do not all lie round the ventricle,
many have moved out to make an elaborate system of cortical layers.
Electrical stimulation of various parts of the optic tectum produces
movements of the limb and other muscles; there can be no doubt
that this region plays a dominant part in behaviour. Most of the fibres
of the optic tract end here, and there are also other pathways from
the olfactory, auditory, medullary (gustatory?), and spinal regions.
Efferent fibres leaving the tectum pass to the midbrain base, medulla,
and perhaps back into the cord. This region therefore has wider con-
nexions than any other part of the nervous system and thus nearly
reaches the status of a dominant integrating organ.

The cerebellum of amphibia, on the other hand, is very small;
perhaps because these are mostly animals that do not have to adjust
themselves freely in space during locomotion, they move mainly in a
single plane. There is little need for control of speed or distance of
movement, except of the head and tongue, which are controlled by
the tectum.

25. Skin receptors

Lateral line organs are present in the skin of all aquatic amphibian
larvae and in some aquatic adults, such as those of the anuran family
Pipidae. They are of simple form, consisting of groups of cells in an

350 AMPHIBIA xn. 25-

open pit. In newts they are present in the larvae, which are aquatic,
but are covered by epidermal layers during the first post-larval stage
during which the newt lives on land. In the final aquatic adult stage
the organs reappear.

The skin, of course, also contains tactile organs, and in addition is
often sensitive to chemical stimuli. This chemical sense is mediated
by fibres running in the spinal nerves, not by special elements such as
the taste-buds found spread out over the body in fishes. The skin is
also sensitive to heat and cold, and there is some evidence that these
senses are served by fibres different from those that mediate touch,
pain, or the chemical senses. Histologically, however, there is little
sign of the development of the special sensory corpuscles that are
so conspicuous in the skin of birds and mammals. All the nerve-
endings are of the type known as 'free nerve-endings', except for a few
touch corpuscles on special regions such as the feet. In this the
amphibia again resemble the fishes and show less differentiation than
do the higher animals.

The taste-buds on the tongue and palate are probably able to
respond to the presence of only two of the four types of substance
that are discriminated by mammals. Applications to the tongue of the
frog and recordings of nerve-impulses in its nerves show that there
are chemoreceptors present able to respond to salt and sour substances,
but that no reaction is given to substances that in mammals are classed
as sweet or bitter.

The olfactory organ functions both on land and in the water, special
mucous glands being present to keep it moist when in air. A continual
circulation of water or air is maintained over the olfactory epithelium
by cilia or the movements of respiration. The internal nostril may
have originally developed from the double nostril of fishes, in order to
make a circulation around the olfactory receptors possible. Jacobson's
organ is a special diverticulum of the olfactory chamber, serving to
test the 'smell' of food in the mouth.

The Apoda, being blind, have a great development of the sense of
smell, including a hollow tentacle or olfactory tube.

26. The eyes of Amphibia

Provided that certain requirements are met the air gives more scope
for the use of photoreceptors than does the water. Light is trans-
ported with less disturbance through the air and image formation is
facilitated by the refraction of the air-corneal surface. The amphibia
have exploited these advantages and sight has become the dominant

xii. 26 THE EYE 351

sense of most of the forms. For clear vision it is essential that the
surface of the eye be protected, kept moist and free of particles, and
for these purposes the eyelids and lachrymal glands are present. The
upper lid is fixed, but the lower is very mobile and folded to make a
transparent structure, the nicitating membrane, able to move rapidly
across the surface of the eye.

C %

Fig. 207. The amphibian eye and its accommodation.

a, anuran eye in vertical section, ac. area centralis; to. inferior oblique; ir. inferior rectus;
//. lower lid; Im. lens muscles (protractors); n. optic nerve; nm. nictitating membrane;
pn. pupillary nodules; sc. scleral cartilage; so. superior oblique; sr. superior rectus; ul. upper
lid; z. zonula Zinnii. b, anterior segment of Bufo in relaxation. C, in accommodation; note
forward movement of lens. (From Walls, after Franz and Ueer.)

The eyeball is almost spherical, with a rounded cornea. The lens is
farther from the cornea than in fishes and is flattened, more so in
anurans than in urodeles. These modifications allow focusing of a
more distant image. There is an iris, with a rapidly moving aperture,
operated by powerful circular (sphincter) and radial (dilatator)
muscles. Although these muscles are partly actuated by a nervous
mechanism they are also directly sensitive to light, and the pupil of
the isolated eye of the frog shows wide excursions with change of
illumination.

Accommodation is effected by protractor lentis muscles, attached
to the fibres by which the lens is supported (Fig. 207). These muscles

352 AMPHIBIA xil. 26-

move the lens forward, whereas the muscles of the lens of teleostean
fishes move it backwards. Other fibres, the musculus tensor chorioi-
deae, run radially and around the lens. They may help the protractors,
and are probably the ancestors of the ciliary muscles of higher
forms.

In amphibia living in the water the eye is based much more on the
fish plan and the lens is rounder. There are then no lids or lachrymal
glands and the eye is enabled to make an image, in spite of the absence
of the air-corneal interface, by a thickening of the inside of the cornea.

Rods and cones are present in the retina, the former containing
visual purple, which may be red or greenish. The two sets of receptor
are apparently found throughout the retina in urodeles, but in Rana
there is a macular region in which the cones are in excess and this is
still further developed in Bufo. Study of the impulses in the optic
nerves of Rana shows that six types of detector operate upon the infor-
mation provided by the rods and cones. (1) Contrast detectors give a
sustained response when a sharp edge moves into the visual field ; (2)
convexity detectors respond to objects that are curved, the discharge
being greater the more curved (smaller) they are. These two types
together may be called 'on' fibres; (3) moving-edge detectors ('on/off'
fibres) respond with a frequency proportional to the velocity of move-
ment; (4) dimming detectors respond on reduction of illumination
('off' fibres); (5) darkness detectors fire with frequency inversely pro-
portional to illumination. These types of fibre project to different
depths in the tectum as sheets of endings, and the arrangement of the
retina is accurately reproduced there although the fibres are interwoven
in the nerve (perhaps to prevent 'cross-talk'). Moreover, if the nerve
is severed the fibres regenerate in such a way as to reconstitute the
map. The sixth type of fibre is sensitive to blue light and is connected
with the thalamus.

These operations serve to provide reports of the types of change
relevant to the animal. Thus the second type might be called 'insect
detectors', responding when a small dark object enters the field
and moves about intermittently. More complex visual discrimina-
tions are also possible, for example toads can distinguish between
shapes.

The skin is probably sensitive to light in all amphibians : frogs react
to light even after removal of the eyes and cerebral hemispheres. This
skin sense is especially developed in certain cave-living urodeles,
Proteus, in which the eyes are not functional. A similar degeneration
also occurs in Apoda.

XII. 27 (353)

27. The ear of Amphibia

The inner ear is divided into a utricle, from which the semicircular
canals arise, and a saccule, from which there is a diverticulum, the
lagena, part of whose receptor surface is covered with a tectorial
membrane somewhat similar to that of mammals. There is, however,
no coiled cochlea. The middle ear of the frog consists of a funnel-
shaped tympanic cavity communicating with the pharynx and closed
externally by a tympanum supported by a tympanic ring. Sound
waves are transmitted across the cavity by a rod, the columella, fitting
by an expanded foot, the otostapes, into the fenestra ovalis, a hole in
the wall of the auditory capsule. This hole is also partly occupied by
a second plate, the operculum, which is joined to the scapula by a
special opercular muscle. The operculum and otostapes develop with-
in the wall of the auditory capsule and the middle part of the colu-
mella (mediostapes) forms as an outgrowth from the otostapes. The
outer part of the columella (extra-columella) and the tympanic ring
develop close to the quadrate and probably from its cartilage.

The columella, therefore, shows no developmental relationships to
the hyoid arch. The tympanic cavity is developed from the spiracular
cleft, after a strange series of changes. The original cleft degenerates
six days after hatching but about six of its lining cells persist and at
the end of the tadpole stage form a tympanic vesicle, which becomes
connected with the pharynx by a rod of cells. This rod then degener-
ates again and an open air passage to the vesicle of the drum is not
established until some thirty days after emergence from the water,
when a pouch from the pharynx joins the tympanic cavity. These
events show the complexities that may result from the modification
of developmental processes, and they emphasize the difficulty in
assigning 'homologies'. It is still debated to what extent the middle
ear of the frog can be compared with that of amniotes. The hyo-
mandibular nerve, which divides above the middle ear of amniotes
(and above the spiracle of the dogfish) lies behind the tympanic cavity
of the frog and branches below it.

The arrangement for conveying vibrations to the ear varies con-
siderably among amphibians. In urodeles there is no tympanum. In
some of them the columella is attached to the squamosal, perhaps in
connexion with a semi-aquatic or burrowing habit. A similar arrange-
ment may have been present in the earliest amphibians, which have
a columella but no oval window. In other urodeles (Plethodontidae)
the columella is attached to the quadrate and there may be a second

354 AMPHIBIA xn. 27-

ossicle, the operculum, working in parallel, with its inner end in the
oval window caudal to the columella and its outer end attached by a
muscle to the scapula. In terrestrial forms the columella becomes fused
with the window at metamorphosis and its function is taken over by
the operculum, probably receiving vibrations from the fore-legs. The
more aquatic forms (Cryptobranchus) retain the larval condition and
never develop an operculum. The tympanum and columella are also
reduced in some terrestrial anurans {Bombinator) but in the aquatic
Xenopus and Pipa the operculum and its muscle are lost, perhaps a
paedomorphic feature.

The sense of hearing is certainly well developed, especially in
Anura, which respond to vibrations from 50 to 10,000 a second. The
hearing is used especially in the breeding-season, when the croaking
serves to attract both sexes to the water. The prey may also be located
by sound. Urodeles have been shown to give no response to the ring-
ing of a bell suspended from the ceiling, which, however, produces
reactions in Rana and Bufo.

A peculiar feature of many Anura is an immense backward develop-
ment of the perilymphatic space of the inner ear, forming a sac
extending above the brain and on either side of the spinal cord as far
back as the sacrum. Portions of this sac emerge between the vertebrae,
showing as whitish masses on account of the granules of chalk they
contain. The calcium salts in these sacs diminish greatly during
metamorphosis and they then refill. The system may serve as a
calcium reserve also for the adult.

28. Behaviour of Amphibia

The habits of amphibia, like their special structures, enable them
to deal with the various emergencies that threaten the continuation of
life on land. Frogs and toads have a strong sense of place and they
show distinct 'homing' reactions. They are able to learn to find their
way out of mazes and to remember the way for periods of at least
thirty days.

Complex migrations are made by many species; nearly all migrate
to the water in spring. In this migration the males usually precede
the females, then attract the latter by their calling. The receptors for
the orientation towards the water are known in the osmoreceptors in
the mouth of the frog. This orientation is particularly clear in uro-
deles, in which sound plays no part in the migration. The power to
find water is obviously of first importance for any animal living on
land, and further study of the receptors involved would be interesting.

xii. 28 BEHAVIOUR 355

The search for food and the avoidance of enemies are not in prin-
ciple more difficult on land than in the water, but they probably
demand new mechanisms. For example, the greater range of visibility
can be a disadvantage, especially when it is exploited by one's success-
ful and predatory descendants. A hawk or owl makes fuller use of its
opportunities in this respect than does the frog, who can only remain
safe from them by behaviour that keeps it concealed. Similarly there
are dangers in certain situations, for instance of desiccation, which
are additional to those that are met by an animal in the water.

In the emergence of the first land vertebrates we thus see a con-
spicuous example of the invasion by living things of a medium far
different from themselves. This produces a situation that calls forth
all the powers of the race to produce new types of individual, and
necessitates that the individuals make full use of their capacities.
New patterns of structure and behaviour are developed as the various
possible situations emerge. The types of organization that at first
manage to survive gradually give place to others, still more complex
or 'higher'. Some traces of the organization of the early venturers can
still be seen in the amphibia, which today exploit the damper situa-
tions on the earth.

XIII

EVOLUTION AND ADAPTIVE RADIATION OF

AMPHIBIA

1 . The earliest Amphibia

There are such close resemblances between the skulls of the earliest
amphibians and those of the Devonian crossopterygian fishes that
there can be no doubt of the relationship (Fig. 194). At present there
is, however, no detailed fossil evidence of the stages of transition
from the one type to the other. The fossils that appear to be closest
to the possible tetrapod ancestor are the osteolepids of the Lower and
Middle Devonian periods, about 375 million years ago. These were
definitely fishes, though they may have breathed air. *Elpistostege is
a single Upper Devonian skull intermediate between such fishes and
the earliest undoubted tetrapods, *Ichthyostega and similar forms,
found recently in freshwater beds of Greenland. These are dated as
very late Devonian or early Carboniferous, that is to say about 350
million years ago. They are the oldest members yet found of the
great group of Stegocephalia, which, throughout the succeeding 100
million years of the Carboniferous and Permian periods, flourished
and developed many different lines, one giving rise to the reptiles and
others to the modern amphibia. The term Stegocephalia is convenient
to cover the whole group of palaeozoic amphibia, all probably of
common descent. At least seven types can be recognized (p. 296), but
attempts to group these have not been altogether successful; the
nomenclature remains confused. The Labyrinthodontia were the central
stock and were in the main terrestrial forms, giving off at intervals lines
that returned to the water. A characteristic labyrinthodont feature is
a folded pattern of the teeth, similar to that of their crossopterygian
ancestors.

The earliest Stegocephalia were definitely tetrapods and already
showed sharp changes from the fish type. *Ichthyostega is known
chiefly from the skull (Fig. 208), which shows all the characteristic
amphibian features, but retained traces of fish ancestry in its shape,
with a short, wide snout and long posterior region (table), and pre-
sence of a preopercular bone. The nostril lies on the very edge of the
upper lip, apparently partly divided by a flange of the maxilla into
internal and external openings.

XIII. 1-2

(357)

2. Terrestrial Palaeozoic Amphibia. Embolomeri and Rhachitomi

We possess more complete information about the slightly later
forms, the Embolomeri, such as *Eogyrinus, from the Lower Carboni-
ferous (Fig. 21 1). These were long-bodied animals, rather newt-like,
and their small limbs cannot have made very effective progress on
land. They probably lived mostly in the water, eating fish. The

Fig. 208. Skull of Ichthyostega. (From Westoll, after Save-Soderbergh.)

d. dentary; en. external nostril; ept. ectopterygoid ; jr. frontal; in. internal nostril; ina.
internasal; /. jugal; la. lachrymal; mx. maxilla; na. nasal; pa. parietal; pal. palatine; pm.
premaxilla; pn. postnarial; po. postorbital; poj. postfrontal; pop. preopercular; ppa. post-
parietal; prj. prefrontal; ps. parasphenoid ; pt. pterygoid; q. quadrate; qj. quadratojugal ;
san. sur-angular; sq. squamosal; sut. supratemporal ; /. tabular; v. vomer.

pectoral girdle was still joined to the skull by a process of the tabular
bone, as in fishes. The pelvic girdle did not form a full articulation
with the sacral vertebrae but was apparently attached only by liga-
ments.

The structure of the vertebrae has given rise to much controversy.
In the earliest amphibia we find three elements, a more dorsal neuro-
pophysis and a centrum composed of two parts, pleurocentrum and
hypocentrum, the latter associated with a ventral arch and rib. These
elements can be identified in the vertebrae of crossopterygians but it
is still not clear what relationship, if any, they have to the two pairs of
vertebral 'arches' alleged to be present in elasmobranchs (see Williams,

J 959)-

Triturus

Fig. 209. Various urodele amphibians, not all to same scale (mostly from life).

xin. 2-3 FOSSIL AMPHIBIA 359

The skull shows the full series of bones that we have already dis-
cussed; there is therefore no reason to suppose that these animals
represent a secondarily 'degenerate' branch, which had returned to
the water. They were probably very close to the ancestors of all
tetrapods. They were numerous in the Carboniferous swamps, but
disappeared early in the Permian. So close were these Embolomeri
to the ancestry of the reptiles that many workers classify them near
the Permian * Seymour ia> which we shall consider as a cotylosaurian
reptile (p. 386).

Throughout the Carboniferous, Permian, and Triassic there were
abundant amphibia of partly terrestrial habit, the Rhachitomi, in
which both vertebral centra were present, the pleurocentrum being
the larger. *Eryops (Fig. 211) was a typical form living in the Permian,
about 250 million years ago. The animals were 5 ft or more in length,
rather like crocodiles, relatively shorter in body and tail than *Eogy-
rinus and with stronger limbs. Nevertheless they probably lived partly
in the water and may have been fish-eaters. The skull was long and
narrow in the front and short in the 'table' behind the eyes, continuing
the previous tendency. A characteristic feature of later labyrinthodonts
now began to appear, namely a dorso-ventral flattening of the skull.
The pectoral girdle was no longer attached to the skull, but there was
a joint between the pelvic girdle and the sacrum. Some Permian
Rhachitomi became still more completely terrestrial than *Eryops,
for instance *Cacops had very large limbs and protective plates along
its back.

3. Aquatic Amphibia of the later Palaeozoic

Other lines of amphibia, however, show an accentuation of the
tendency to return to the water. In the vertebrae the anterior hypo-
centrum became large, while the pleurocentrum disappeared. At the
same time the skull became very flattened and the limbs weak. Several
stages are known leading from the Rhachitomi to these fully aquatic
forms of the Trias, which are placed in the suborder Stereospondyli.
*Capitosaurus and *Buettneria are typical of the group, which
remained numerous until near the end of the Triassic period, about
150 million years ago. Probably this change from rhachitomous to
stereospondvlous condition occurred on several independent lines of
descent. Thus amphibia, after becoming semi-terrestrial in the Car-
boniferous and then probably giving rise to the early reptiles, later
returned to the water.

We also have record of various other secondarily aquatic amphi-

(36o)

Ascaphus

Breviceps

Polype dates

Ran a

Fig. 210. Various anuran amphibians, not all to one scale.

(Ascaphus, Nectophrynoides, and Polypedates after Noble, Breviceps after Thompson,
Gastrotheca after B.M. Guide, others from life.)

xiii. 3 AQUATIC AMPHIBIA 361

bians whose affinities are less certain. They have in common a reduc-
tion of ossification in general and in particular in the centra, which
seem not to be formed from separate cartilaginous elements as in
labyrinthodonts but as thin continuous sheets of bone. Some of these
animals classed as Phyllospondyli or 'Branchiosaurs' were almost
certainly larval Rhachitomi; the external gills can be recognized and
stages found connecting them with known adults of that group. It is
necessary, however, to retain the order for the present.

Other early aquatic amphibia are less easy to classify and are
grouped for convenience as an order Lepospondyli, all having verte-
brae composed of a single piece, and a continuous notochord. They
show, however, at least three distinct lines, probably separate off-
shoots from the main labyrinthodont stock. *Dolichosoma and other
forms from the Carboniferous were like snakes and had lost the limbs.
*Diplocaulus from the Permian possessed remarkable horned skulls.
These creatures with broad flat heads and upward-looking eyes and
small limbs were presumably bottom-dwellers and the development
parallels that of the Stereospondyli. A third aberrant group placed
here, the Microsaurs, such as *Microbrachis, were animals with long
bodies and small limbs, presumably aquatic, but showing many
similarities to the reptiles in the skull.

The order Adelospondyli has been created for a further collection
of presumably secondarily aquatic amphibia such as *Lysorophus, in
which the neural arch and centrum are not fused but articulate by
means of a jagged suture. The skull shows reduction and variation
of the bones, and for this and other reasons it has been suggested that
the urodeles may have arisen from an adelospondylous line.

The relationship of the modern amphibia to these palaeozoic
stegocephalians remains uncertain. The earliest anuran is *Proto-
batrachus of the Triassic, possessing ribs and a tail, but with elongated
ilia and an anuran type of skull. It is probably a larva in metamor-
phosis. *Miobatrachus of the Carboniferous is a form in which the
posterior portion of the skull is shortened and the temporal bones lost.
In other respects the skull is like that of a rhachitome and suggests
that the frogs diverged from the labyrinthodonts at this very early
stage.

The urodeles can be traced back only to the Jurassic. It is often
suggested that both they and the Apoda have arisen from aquatic
Lepospondyli, such as the microsaurs, but there is no real evidence
of this.

362 AMPHIBIA xiii. 4

4. Tendencies in the evolution of fossil Amphibia

The changes in the form of amphibia can be followed from the
beginning of the Carboniferous to the end of the Triassic period, and,
indeed, in the form of their reptilian descendants far beyond. There
are signs, however, of very many distinct lines (as we should expect),
and it is not possible to trace details of the history or fate of par-
tieular populations. Two distinct tendencies appear over this period:
(i) to become fully terrestrial, (2) to return to the water. The terres-
trial forms became very gradually shorter in body and stronger in leg.
The skull remained fairly high and domed and the otic notch became
deeper, as a more effective tympanum developed. In the vertebrae
the hypocentrum became reduced as muscles developed attached to
the pleurocentrum.

Return to the water led to animals of two distinct types, (a) snake-
like or (b) flattened, but in both there was a reduction of limbs and
a secondary lengthening of the body, with return to the sinuous
movements of fish-like locomotion. In the bottom-living forms, such
as some Stereospondyli and *Diplocaahis among Lepospondyli, the
skull became flattened, with the eyes looking upwards, the otic notch
being shallow. The snake-like *Dolichosoma retained the more normal
skull shape but became immensely elongated and lost the limbs
altogether.

These observed tendencies can be understood to result from the
situation that developed as the vertebrates first colonized the land.
The earlier amphibia, such as *Eogyrinus, were partly aquatic, by
force, one might say, of inexperience. Throughout the Carboniferous
various lines of them became more fully equipped for terrestrial life,
moving faster, seeing and hearing better, and so on. The competition
and predatory attacks of these more successful lines then drove others
back into the water and so the process continued, until later the earlier
reptilian lines, themselves driven back to the water by their own
descendants, removed most of the amphibians from the waters as
well as from the land, leaving only some few remaining populations,
from which the modern orders have evolved.

It certainly does not seem necessary to postulate any special
directive force to explain all this. We could wish, of course, for
much more information, but it seems reasonable to imagine that
these changes were produced by the action of the animals with each
other and with the environment, supposing that the animals con-
tinually strive to feed, grow, and reproduce others rather, but not
quite, like themselves.

(363)

Ichthyophis

Fig. 2ii. Chart of evolution of amphibia.

364 AMPHIBIA xiii. 4-

It must be stated, however, that Watson, who has contributed more
than anyone to knowledge of amphibian evolution, believes that it is
possible to recognize a number of non-adaptive trends, which are
independent of environmental influences. Changes suggested by
Watson and others as non-adaptive include flattening of the skull,
doubling of the occipital condyles, reduction of the number of roofing
bones and loss of ossification in the neurocranium, the changes in the
vertebrae already mentioned, and many other features. It is not
entirely clear how the 'non-adaptive' nature of these features is estab-
lished. SevertzofT has suggested that the flattening of the head is
connected with the development of a large mouth for buccal respira-
tion. Palaeontology necessarily deals with small points of structure,
whose significance for the animal may be difficult to determine, but
it does not follow because we are not able to discern the significance
of a part that it therefore has none. It is not at all easy in biology to
hold the balance between credulous acceptance of a function for
every character and a sceptical attitude that insists on regarding the
organic world as a jumble of unrelated substances. The only safe rule
is to search continually for signs of regular recurrence of similarities
of structure and action, and then to make hypotheses about function,
which can be tested by experiment.

5. Newts and Salamanders. Subclass Urodela

The urodeles, also called Caudata or tailed amphibia, show less
deviation from the general form and habitats of the amphibia as a
whole than do the specialized anurans (Fig. 209). The adult and larval
urodeles differ little from each other, and characters suitable for
aquatic life are frequently found in the adult. Indeed, all stages of
suitability for land occur, from the terrestrial salamanders, such as
Salamandra maculosa, the European salamander, which is viviparous,
to the fully aquatic forms, for instance Necturus, the mud-puppy of
North America. In many of the aquatic animals there is a tendency to
retain in the adult characters usually found in larvae. This process of
paedomorphosis has developed to various extents, and independently
in several groups. Thus the giant salamander Megalobatrachus, 5! ft
in length, in China and Japan, has no eyelids, but loses its gills in
the adult. In Cryptobranchus, the hell bender of the United States,
the spiracle remains open and is used for the outlet of water during
respiration.

Amphiuma, also from the southern U.S.A., is a very elongate form,
with absurdly small legs, no eyelids, and four branchial arches. In

xiii. 6 MODERN AMPHIBIA 365

the still more modified forms, such as Necturus, external gills are
present and the lung is so reduced that the animals can live walking
along the bottom. Proteus from European caves is a blind urodele
with external gills and no pigment. Siren shows almost entirely larval
characteristics and has no hind limbs.

The more typical terrestrial newts are of several sorts. In North
America the common genus Amby stoma (usually written Amblystoma)
has eleven species, many adapted to special habits, including A. mexi-
canum, in which some races become mature without metamorphosis,
because of lack of iodine in the water, whereas others, the axolotls of
Mexico, are genetically neotenous.

The common British newt Triturus vulgaris is a typical example of
the more definitely terrestrial urodeles, though it is not able to live in
very dry situations. However, the limbs support much of the weight
of the body, and their soles are applied to the ground and turned
forwards. The tail shows various degrees of reduction to a circular
organ, but in the breeding-season, when both sexes return to the
water, it develops a large fin, especially in the male. The common
newts of America form a distinct family, including Plethodon and
many specialized forms, such as the blind Typhlomolge, inhabiting the
waters of caves.

6. Frogs and Toads. Subclass Anura

Among the frogs and toads are very many suited for special modes
of life, and it must again be emphasized that this is far from being a
static and precariously surviving group. We have already mentioned
the frog Ascaphns, which lives in mountain streams in the north-west
of the United States and has reduced lungs, showing a combination
of specialized and primitive features. Internal fertilization is assured
by a penis-like extension of the cloaca. In this genus and the New
Zealand Leiopelma (Fig. 210) there are several primitive features,
including tail muscles (absent in all other anurans), amphicoelous
vertebrae, free ribs, abdominal ribs, and persistent posterior cardinal
veins.

In Alytes y the midwife toad of Europe, the male carries the eggs
wrapped round the legs. Pipa is a related and still more specialized
aquatic frog from South America; it has no tongue, and, curiously
enough, has developed an elaborate arrangement by which the young
are carried in pits on the back. Xenopus of Africa is related to Pipa,
but without the habit of carrying its young (Fig. 210).

The bufonid toads are among the most successful of all amphibian

366 AMPHIBIA xm. 6-

groups and are more fully adapted than most for a terrestrial life, but
return nearly always to the water to breed. Bufo itself is found in
almost all possible parts except in Australia and Madagascar; related
genera, many of them with special features, are found all over the
world. Curiously enough only one genus, Nectophrynoides from East
Africa, is viviparous, the young being in that case provided with a
long vascular tail, by means of which they maintain contact with the
wall of the 'uterus', even though embedded in a mass of embryos.

Hyla and other tree-frogs, very widely distributed, are similar to
the bufonids but have pads on the toes by which they climb, and
many other adaptations to arboreal life. Gastrotheca (= Nototrema),
the marsupial frog, is a genus in which the young develop in a sac on
the back of the female, this sac being in one species protected by
special calcareous plates. Rana and its allies, the true frogs, are also
cosmopolitan. A number of frogs related to Rana have taken to a tree-
living habit, developing pads on the toes. Polypedates is a widespread
genus and there are several others, each independently derived from
ranids. This is therefore a striking illustration of parallel evolution —
the hylid tree-frogs having arisen from bufonids and probably several
sorts of polypedatids from ranids.

Burrowing with the legs has also been evolved several times by
anurans. In Breviceps (Fig. 210), which digs for ants, there is a large
snout, as in other anteaters.

7. Subclass Apoda (= Gymnophiona = Caecilia)

These (such as Ichthyophis) are burrowing, limbless creatures living
like earthworms, in the tropics. They show several interesting primi-
tive features, including the retention of small scales in the skin. They
are specialized, however, in having a very short tail and some features
suited to their terrestrial life, such as copulatory organs. The animals
are blind, the place of the eyes being taken by special sensory ten-
tacles. The eggs are large and yolky and cleavage is meroblastic; they
are laid on land and the embryos develop around the yolk sac, but
often have long, plumed gills. Vivipary is common, including in the
aquatic form Typhlonectes.

8. Adaptive radiation and parallel evolution in modern Amphibia

Even this superficial study of the 250 genera and about 2,000 species
of modern amphibians shows that the features we have already
recognized in fish evolution are found also in evolution on land. It is
difficult in a short time to gain an impression of the very great variety

xiii. 9 AMPHIBIAN EVOLUTION 367

that is characteristic of any group of animals when closely studied.
Besides the main types that can be distinguished, countless lesser
variations will be found, and one realizes that the characteristics of the
populations are still today in process of continual and perhaps rapid
change. Anyone trying to discover the relationships of the various
derivatives of ranids or bufonids must be impressed by the presence
of series of parallel lines of development, so that it is impossible to
disentangle the relationships. Evolution viewed at close quarters by
the student of abundant modern animals looks very different from
the simple picture seen by the lucky collector of a few rare fossils,
who can arrange his types in genealogical trees and is apt to forget that
they represent only an infinitesimally small sample of abundant and
varied populations.

We can perhaps find certain tendencies in the modern amphibian
populations that are similar to the tendencies of the fossil series. Many
return to the water, especially among the urodeles. Others become
more fully terrestrial, either by climbing trees or by burrowing into
the earth. Both these habits have been independently adopted many
times by recently evolved lines and, no doubt, still more often in the
past by creatures that have died out, leaving no trace.

9. Can Amphibia be said to be higher animals than fishes?

It is not easy to decide whether there is a clear sense in which
amphibians can be said to have advanced over their fish ancestors.
They have moved from the water into environments that are in a
sense less suitable for life. In order to maintain a watery system, such
as a frog or toad, outside the water, various special structures and
methods of behaviour have been evolved. The presence of such
additional systems can be said to add complexity to the organization.
It is difficult to make a count of the number of 'parts' involved in the
organization of any animal. Amphibia possess many special devices,
for instance, for respiration without loss of moisture, for control of
water intake and water loss, for return to water to breed, and so on.
Even without making a proper quantitative computation it seems
reasonable to say that these add up to make an organization more
complicated than that of a fish. The integration of the action of so
many parts requires an elaborate nervous system, and there is evi-
dently some connexion between the increased size and importance of
the nervous system and the development of this more complicated
organization that enables life to continue in a different environment.

Considering the matter in this way it is hardly sensible to ask the

368 AMPHIBIA xm. 9

question 'Are the amphibians more efficient than the fishes?', the
work that they do in maintaining life is so different that a comparison
of 'efficiency' is fallacious. One method of assessing living efficiency
might be to judge each animal organization by the extent to which it
maintains its constancy — by its power of homeostasis. Data about the
fluctuations of the internal environment are so scanty among lower
vertebrates that we cannot proceed very far on these lines. It is
probable that the blood of fishes shows greater fluctuations, for
instance in osmotic pressure or lactic acid content, than does that of
amphibians, such fluctuations being perhaps even an advantage in
allowing life in waters of differing salinity. In fact, to say that the
whole mechanism of homeostasis becomes more complicated in land
animals is only to say over again that they are 'higher' because they
have more special work to do to maintain themselves in a difficult
environment. Almost every part of the body shows signs of this greater
complexity; the central nervous system becomes larger, the autonomic
nervous system develops more elaborate control of the viscera. The
endocrine glands become more numerous and differentiated, the
muscular system shows more distinct parts, enabling the animal to
act in new ways.

However difficult such comparisons may be it is hardly possible
to deny them some validity. Amphibian organization differs from
that of fishes and may be said to be 'higher' in the sense that it is more
elaborate and allows life in conditions that the fish organization
cannot tolerate.

XIV

LIFE ON I AND: THE REPTILES

1 . Classification

Class. Reptilia
Subclass i. Anapsida

Order i. *Cotylosauria. Carboniferous-Trias

*Seymouria; *Captorhimis; *Diadectes
Order 2. Chelonia. Permian-Recent

*Eunotosaurus; *Triassochelys; Chelys; Emys; Chelone;

Testudo

Subclass 2. *Synaptosauria

Order 1. *Protorosauria. Permian-Trias

*Araeoscelis; * Tanystropheus
Order 2. *Sauropterygia. Trias-Cretaceous

*Lariosaurus; *PHosaurus; *Plesiosaurus; *Placodus

Subclass 3. # Ichthyopterygia

Order 1. *Ichthyosauria. Trias-Cretaceous
*Mixosaurus; * Ichthyosaurus

Subclass 4. Lepidosauria

Order 1. *Eosuchia. Permian-Eocene

* Yoimgina; *Prolacerta
Order 2. Rhynchocephalia. Trias-Recent

*Homoesaurus; * Rhynchosaurus ; Sphenodon (= Hatteria)
Order 3. Squamata. Trias-Recent

Suborder 1. Lacertilia (= Sauria). Trias-Recent
Infraorder 1. Gekkota. Mainly Recent

Gecko
Infraorder 2. Iguania. Cretaceous-Recent
Iguana; Anolis; Phrynosoma; Draco; Lyriocephahis ; Agama;

Chamaeleo
Infraorder 3. Scincomorpha. Eocene-Recent
Lacerta; Scincus; Amphisbaena
Infraorder 4. Anguimorpha. Cretaceous-Recent
*Dolichosaurus; * Aigialosaurus ; *Tylosaurus; Varanus; Lan-
thanotus; Atwuis

37°

REPTILES xiv. i-

1. Classification {cont.)

Suborder 2. Ophidia (= Serpentes). Cretaceous-Recent
*Palaeophis; Python; Natrix; Naja; Vipera

Subclass 5. Archosauria

Order 1. *Pseudosuchia (= *Thecodontia). Trias

*Enparkeria; *Saltoposuchns
Order 2. *Phytosauria. Trias

*Phytosaurus; *Mystriosuchus
Order 3. Crocodilia. Trias-Recent

*Protosuchus; Crocodilus; Alligator; Caiman; Gavialis
Order 4. *Saurischia. Trias-Cretaceous
Suborder 1. *Theropoda

*Compsog?iathus; *Ornitholestes; * Allosaurns ; *Tyranno-
saurus; * Strnthiomimus
Suborder 2. *Sauropoda
*Apatosaurus (= *Brontosaurus); *Diplodocus; *Yaleosaurus;
*Plateosanrus; Brachiosaurus
Order 5. *Ornithischia. Trias-Cretaceous
Suborder 1. *Ornithopoda

*Camptosaurus; *Iguanodon; *Hadrosaurus
Suborder 2. # Stegosauria

* Stegosaurns
Suborder 3. *Ankylosauria

* Ankylosaurus ; *Nodosanrus
Suborder 4. *Ceratopsia

* Triceratops

Order 6. *Pterosauria. Jurassic-Cretaceous
*Rhamphorhynchns ; *Pteranodon

Subclass 6. *Synapsida. Carboniferous-Permian

Order 1. # Pelycosauria (= # Theromorpha)

* Varanosaurus; *Edaphosaurus; *Dimetrodon
Order 2. *Therapsida. Permian-Jurassic

*Scym?iognathus; *Cyiiognathus; *Bauria; *Dromatherium;
* Dicynodon
Order 3. *Mesosauria (— Proganosauria). Permian
*Mesosaurus

xiv. 2 (370

2. Reptilia

Towards the end of the Devonian period, say 350 million years
ago, the vertebrate organization produced a population of amphibian
creatures and from this has been derived not only various modern
groups classed as amphibia but also the more fully terrestrial popula-
tions that do not need to breed in water — the Amniota. Since that
time many divergent lines have evolved from this stock, including the
birds and the mammals, and it is evident, therefore, that it is likely to
be difficult to specify what is meant by a reptile, as distinct from an
amphibian or a bird or mammal. The term does not define a single
vertical line of development or branch of an evolutionary tree, but
is rather a horizontal division, marking a band on the evolutionary
bush, specifying a level of organization beyond that of an amphibian
but before that of either bird or mammal. Attempts have been made
to divide the reptiles vertically into sauropsidan (bird-like) and
theropsidan (mammal-like) lines, but such a division, although it has
some foundation, obscures the fact that their bush-like evolutionary
radiation has produced not two but many types.

The existing reptiles belong to four out of the dozen or more main
lines that have existed. The most successful modern forms are placed
in the order Squamata, the lizards and snakes, the latter being of
relatively recent appearance in their present state. Secondly, the
tuatara, Sphenodon, of New Zealand is a relic surviving with little
change from the Triassic beginnings of this group. Thirdly, the
crocodiles are an older offshoot from the stock from which the modern
birds were derived. Finally the tortoises and turtles (Chelonia) have
retained in some respects the organization of still earlier times,
perhaps through the special protection of their shells. Though they
are much modified in some ways, they still show us several character-
istics of the earliest Permian reptiles.

These four modern types are all that remain of the reptiles that
flourished throughout the Mesozoic, culminating in the giant dino-
saurs of the Jurassic and Cretaceous. Evidently a profound change
affected the population of the world, including the sea, between the end
of the Cretaceous and the Eocene. This change will be discussed
further in Chapter XXI, but we must briefly discuss here the possible
relation of the decline of the reptile populations to the rise of their
descendants, the birds and mammals. It can hardly have been only
the more efficient organization due to the warm blood that gave
these their opportunity, for there were forms in the Trias so similar

372 REPTILES xiv. z-

to mammals in their skeletons that we may reasonably (though
not certainly) suppose them to have been warm-blooded. There were
birds with feathers in the Jurassic, and it is probable that they also
already had warm blood. However, as a working hypothesis, we may
suppose that the climate, which had been suitable for reptiles in the
Mesozoic, became less so in the early Tertiary, and the most obvious
suggestion is that colder conditions developed all over the earth's
surface. The modern reptiles for the most part live in the temperate
and tropical zones, indeed they flourish only in the latter. However, it
must be remembered that climate fluctuates continually (p. 13); it is
dangerous to make generalizations about conditions over such long
periods as the Cretaceous.

3. The organization of reptiles

The organization we call reptilian is, generally speaking, suitable for
life in warm countries, though two species, the common lizard
(Lacerta vivipara) and the adder ( Vipera berus), are found as far north
as the Arctic Circle. No doubt the distribution of reptiles is limited
largely by the fact that they cannot maintain a temperature above that
of the surroundings by production of heat from within. The wide-
spread idea that reptiles have no means of regulating their body
temperature, however, has been overemphasized. Bogert and his
collaborators in the U.S.A. have shown that in the wild (though not
as a rule under laboratory conditions) reptiles are often able by suitable
behaviour to maintain their body temperatures at a remarkably high
and constant level throughout much of the day, by varying their
exposure to the available sources of heat. When they get cold they
bask in the sun or rest on warm rocks; when they get too hot they
shelter under vegetation or in holes. In some species, too, colour
change plays a part in temperature control, the animals becoming
darker or lighter in colour, according to whether heat absorption or
reflection is the appropriate response.

It has also been shown that each species of reptile has an optimum
range of temperature, below which the animals become inactive and
above which they quickly die. In some desert lizards the upper limit is
above 40 C. The range tends, as one would expect, to be higher in
diurnal than nocturnal forms, and is in general higher in lizards than
it is in snakes or alligators.

The reptilian method of temperature control differs essentially
from that of mammals in that it depends on the availability of external
sources of heat such as the sun, rather than on the ability to conserve

xiv. 5 SKIN OF REPTILES 373

or lose heat generated within the body. For this reason reptiles are
sometimes termed 'ectothermic' and mammals 'endothermic'. These
terms are perhaps preferable to 'poikilothermic' (having a variable
temperature) and 'homoiothermic' (having a constant temperature)
which are in more general use.

The ectothermic method of temperature control presupposes some
sensitive mechanism for registering slight changes in the temperature
of the surroundings. There is evidence that the pineal complex is the
receptor and that the hypothalamus may be involved in thermal
homeostasis.

It remains true to say, however, that no reptile can retain an inde-
pendent body temperature for a long period. For this reason, reptiles
living in temperate climes must hibernate during the winter, while in
warm countries some, conversely, aestivate during the hottest months.

4. Skin of reptiles

The skin is characteristically dry; unlike the skin of amphibians and
mammals it contains few or no glands. The Malphigian layer of the
epidermis produces the horny scales, which are periodically shed in
flakes, or, as in snakes, cast as a single slough. Beneath the horny
scales many reptiles (some lizards, crocodiles, some dinosaurs) develop
bony plates in the dermis (called osteoderms). These may be re-
stricted to the head, where they lie superficial to the skull bones, or
may cover most of the body. The tortoise's shell contains both horny
(epidermal) and bony (dermal) components (p. 394). The horny
scales are often modified to form crests, spines and other appendages.

Many reptiles, particularly lizards and snakes, have bold and
elaborate colour patterns. These may play a part in concealment
(though they often seem conspicuous in captive specimens away from
their normal terrain). In some forms, especially lizards, there are
marked colour differences between the sexes (see p. 407). The well-
known phenomenon of colour change, which is much more marked
in certain lizards than in any other known reptiles, is discussed on
p. 410.

5. Posture, locomotion, and skeleton

The elongated body and small laterally projecting legs of many
reptiles recall those of a urodele, and the method of locomotion is in
general similar in the two groups. Many retain the primitive five digits
in both hand and foot. With the similarity of movement goes a general
similarity in plan of the skeleton: there are, however, certain most

374 REPTILES xiv. 5

significant features, characteristic of the reptiles. The head is carried
off the ground, on a well-developed neck. The two first cervical
vertebrae are modified to form the atlas and axis. The atlas is a ring
of bone without centrum, but with a facet in front for the occipital
condyle and one behind for the odontoid process, a peg attached to
the front of the axis but derived in development from the centrum of
the atlas segment.

-sc.

Fig. 212. Shoulder girdle and sternum of a lizard (Iguana).

el. clavicle; cor. coracoid; gl. glenoid; int.cl. interclavicle; pr. procoracoid
process; sc. scapula; st.r. sternal rib; St. sternum. (From Reynolds, after Parker.)

The vertebrae articulate with each other by a system of interlocking
processes much more elaborate than that found in fish-like vertebrates
and presumably serving to allow the column to carry weight. As a
rule, each centrum is concave in front, covering the convex hind end
of the vertebra next to it, a condition known as procoelous. In aquatic
vertebrates the centra articulate by flat surfaces and this condition was
retained in the amphicoelous vertebrae of many primitive reptiles.
Besides this articulation of the centra the vertebrae are also united by
the zygapophyses, facets on the neural arches, so arranged that the
upwardly facing surfaces of the anterior zygapophyses slide over the
down-facing surfaces of the posterior zygapophyses, an arrangement
that is found throughout the amniotes.

Ribs are well developed in the middle or trunk region; each arti-
culates with the body of the vertebra by a single capitular facet.

xiv. 5 GIRDLES AND LIMBS 375

The vertebrae can often be divided into four sets. The cervical
vertebrae, which are very variable in number, have short ribs, not
reaching the sternum. Sternal ribs occur in the thoraco-lumbar seg-
ments (Fig. 212). The ribs of the two sacral vertebrae are short and
broad and articulate with the ilia. The numerous caudal vertebrae
show reduction of all parts, especially towards the tip of the tail. The
chevron bones are ossicles attached to the caudal centra and represent-
ing the reduced intercentra.

The girdles and limbs (Figs. 183-6 and 212) show the same general
structural and functional features as those of amphibia. The limbs
form the main locomotor system, the metachronal contraction of the
myotomes playing a lesser part than in urodele amphibians. The
humerus and femur are normally held in such a position that their
outer ends lie higher than the inner, that is to say, in a position of
abduction. The radius and ulna and tibia and fibula proceed down-
wards towards the ground (at right angles to the proximal bones) and
the hand and foot are turned outwards at right angles, to rest on the
ground. The main muscles thus draw the humerus and femur back-
wards and forwards as well as downwards, and the ventral regions of
the girdles are large and flattened to receive these muscles; in mam-
mals, with a different system of progression, the more dorsal parts
of the girdles have become developed.

The pectoral girdle (Figs. 183, 212) consists of a dorsal scapula and
a large ventral coracoid, which may be fenestrated. Distinct pro- and
post-coracoid elements are probably only found in the extinct mam-
mal-like reptiles. The dermal components are represented by the
paired clavicles and median interclavicle. A cleithrum is found in a
few very primitive forms.

In the pelvic girdle (Fig. 184) the usual dorsal ilium, anterior pubis,
and posterior ischium are found, the last two meeting their fellows in
midline symphysis.

The characteristic modifications of the reptilian skull are discussed
on p. 391. The general plan is similar to that of primitive amphibians,
but in all except the most primitive reptiles there is a development of
holes (fossae) in the temporal region to provide space for the bulging
temporal muscles. The skull roof is in some respects more primitive
than that in modern amphibians (Figs. 213 and 214). It is made up of a
large series of dermal bones, including the nasals, prefrontals, frontals,
supra-orbitals, and parietals. The side of the skull is usually less com-
plete, composed of the tooth-bearing premaxillaand maxilla, lacrymal,
jugal, post-orbital, squamosal, supratemporal and quadrate. The

376 REPTILES xiv. 5

naming of some of the smaller bones round the orbit and above
the quadrate is a matter of controversy.

The margins of the palate are formed by flanges of the premaxillae

Fig. 213. Skull and lower jaw of Lacerta.

A, dorsal view; 13, ventral view; C, from left side; D, right half of lower jaw from inner
side, showing the pleurodont arrangement of the teeth. E.P. ectopterygoid; Ep.P. epiptery-
goid; F, Fr. frontal ; jug. jugal; Lac. lachrymal; Max. maxillary; N, Na. nasal; N, in B,
inner narial opening; Pal. palatine; Par. parietal; Pmx. premaxillary ; Pr.f. prefrontal;
Pt.f. post-orbital; Pt.f 2 . post-frontal; Ptg. pterygoid; Q. quadrate; S.ang. supra-angular;
Sq. squamosal; '. 'o. vomer. The regions of persistent cartilage are not shown in detail.

(After Gadow.)

and maxillae and the small ectopterygoids. The internal nostrils
usually lie forwards between the maxillae, vomers, and palatines.
More posteriorly the floor of the skull is made up mainly by pterygoid
bones and the parasphenoid, which is partly fused with the lower
surface of the basisphenoid. Occipital bones surround the foramen
magnum and make up the single occipital condyle, which in some

xiv. 5 SKULL 377

forms is indented to form three partly distinet lobes. In many reptiles
there is an epipterygoid bone on either side of the brain-case behind
the orbits; this is regarded as an ossification in the ascending process
of the palato-quadrate. The lower jaw usually consists of six bones,
the articular forming the joint with the quadrate, and the dentary
carrying teeth.

The anterior part of the chondrocranium, surrounding the front of
the brain, and the nasal capsule, remain more or less unossified, and

Fig. 214. Diagram of the skull of lizard to show temporal fossa.

a. articular; an. angular; bo. basioccipital; bs. basisphenoid; c. coronoid; d. dentary; da.
dermal articular; do. dermal supraoccipital; ept. ectopterygoid; eo. exoccipital ; fr. frontal;
j. jugal; /. lachrymal; mx. maxilla; n. nostril; na. nasal; o. orbit; op. opisthotic; pa. parietal;
pal. palatine; pv. prevomcr; pm. premaxilla; po. post-orbital; pof. post-frontal; pr. pro-otic
pra. prearticular; pr}. prefrontal ;ps. presphenoid; pt. pterygoid; q. quadrate; qj. quadrato-
jugal; sa. surangular; sf. upper temporal fossa (this is shown diagrammatically, as it occurs
in many lizards; in Lacerta it is largely covered by an extension of the post-frontal — see
Fig. 213); so. supraoccipital; sp. splenial; sq. squamosal; St. supratemporal; v. vomer.

(From Goodrich.)

in places may be membranous. There may, however, be small ossified
orbitosphenoids and farther back pleuro- or laterosphenoids, which
develop in the pila pro-otica uniting the orbital cartilage with the
otic capsules. Between the eyes there is in most reptiles a thin sheet
of cartilage known as the interorbital septum, which may be partly
ossified by small presphenoid elements. The posterior part of the
chondrocranium ossifies to form the following bones; occipital com-
plex, basisphenoid, and the ossifications in the otic capsule (pro-otic,
opisthotic, &c).

In many reptiles the upper jaw and front part of the skull can move
to some extent in relation to the occipital region and cranial base,
such movement being termed kinesis (p. 405). This is often associated
with mobility of the quadrate, as in lizards, snakes, and certain dino-
saurs. Kinesis helps to widen the gape and may provide a shock-
absorbing effect when the jaws are snapped together.

The postmandibular visceral arches play no part in jaw support but
are incorporated into the ear and hyoid apparatus. There is a rod-like

378 REPTILES xiv. 5-

columella auris with a small cartilaginous element (extra-columella)
at its outer end. The columellar system usually conducts vibrations
from the tympanum, lying behind the quadrate, to the fenestra ovalis
and inner ear. In some forms, e.g. snakes, however, the tympanum is
absent and the outer end of the columella is applied to the quadrate.
These animals may be deaf to air-borne sounds but sensitive to
ground vibrations, transmitted through the bones of the jaw.

The hyoid apparatus consists of a basal plate, which projects into
the tongue, and three pairs of ascending horns. These represent the
remains of the hyoid and branchial arches.

6. Feeding and digestion

Food is seized either by the teeth or, in some specialized lizards
such as the chameleon, with the elongated tongue. The teeth are
situated along the edges of the jaws and often also on some of the
bones of the palate. Typically, they are all of the same conical shape,
but may be slightly serrated, or modified to form crushing plates,
poison fangs, and other devices. As a rule, tooth succession is con-
tinuous throughout life, though exceptions to this are found among
the lizards. Salivary glands are well developed in some forms; in
snakes and one genus of lizards (Heloderma) some of them are modified
to form poison-glands. The tongue is very variable, being hardly
movable in some reptiles (e.g. crocodiles) but long, forked, and highly
mobile in others (e.g. snakes).

Digestion proper begins in the stomach. The alimentary canal is
built on the typical vertebrate plan, with a tubular stomach, rather
short small intestine, and wider large intestine, leading to a short
caecum.

There is a well-marked cloacal chamber in all reptiles, subdivided
into a coprodaeum for the faeces, and a urodaeum for the products of
the kidneys and genital organs. These two chambers open into a final
common proctodaeum, closed by a cloacal sphincter. This division
of the cloaca is associated with the necessity for the retention of water,
the cloacal chambers serving for water reabsorption from both the
faeces and urinary excreta (p. 380).

7. Respiration, circulation, and excretion

The typical method of respiration is a backward movement of the
ribs, produced by the muscles attached to them. There is no complete
separation of the thorax from the abdomen, but a partial diaphragm
may be present. The glottis is a slit at the back of the mouth and leads

xiv. 7 CIRCULATION 379

into a larynx with supporting cricoid and arytenoid cartilages. Many
reptiles are able to produce small sounds, but the voice-box is less
developed than in either amphibia or birds.

The lungs are sacs whose walls are folded into ridges, separating
a number of chambers or bronchioles. The hinder part of the lung is

car. int.

car. ex t.

Fig. 215. Diagram of heart and arteries of Lacerta.

car.ext. external carotid; car. int. internal carotid; c.car. common carotid; coel. coeliac artery;

d.a. dorsal aorta; d.B. ductus Botalli (arteriosus); d.car. ductus caroticus; l.aur. left auricle;

p.a. pulmonary artery; p.v. pulmonary vein; r.aur. right auricle; scl. subclavian artery;

sept, interventricular septum; v.c. eaval veins. (From Ihle, after Goodrich.}

nearly smooth and in some lizards, as in birds, it becomes developed
into characteristic air sacs. The tendency is for the more anterior por-
tion of the lung to become the effective vascular and respiratory region,
allowing the air-stream to be drawn across it at both inspiration and
expiration.

The circulation (Fig. 215) of lizards shows a partial separation of
venous and arterial blood; there are two auricles, but only one ven-
tricle, this being partly divided by a septum into right and left sides.
Three arterial trunks arise directly from the ventricle, these being the

380 REPTILES xiv. 7-

right and left aortae, and the pulmonary trunk. The opening of the
latter lies opposite the right side of the ventricle and receives pre-
dominantly venous blood. The left systemic arch opens opposite to
the incomplete ventricular septum and receives mixed blood, whereas
the right systemic arch opens from the left side of the ventricle and
carries almost pure arterial blood. The carotid arteries of both sides
arise from the right systemic arch. This 'classical' view of the cir-
culation of the blood in the reptilian heart has recently been confirmed
by the radiographical studies of Foxon and his colleagues on the green
lizard. Variations may be found, however, in different species.

The venous system is based on the same plan as that of the frog,
with pelvic veins receiving blood from the tail and hind legs and
returning it to the heart through either an anterior abdominal vein
or renal portals, and the inferior vena cava.

In the urinogenital system is seen another feature characteristic of
amniotes, the development of a posterior region, the metanephros,
concerned solely with excretion, leaving the mesonephric (Wolffian)
duct to function as the vas deferens in the male. There is sometimes
an endodermal (allantoic) bladder.

The waste nitrogen is largely excreted as uric acid and this allows
the reabsorption of much of the water in the urodaeum, with precipita-
tion of the organic matter as a chalky white mass of urates. The
advantage of this method of excretion is that it allows for a greater
economy of water than would be possible if the end product was the
more soluble urea. There is, however, some variation in the mode of
excretion among certain members of the group and this may depend
on the manner of life of the species and the necessity for water con-
servation. Thus among Chelonia the more aquatic forms (Emys) pro-
duce considerable amounts of ammonia and urea, but relatively little
uric acid, whereas the last is the main excretory product of the fully
terrestrial types, such as the Grecian tortoise (Testudo gracca), which
can live under almost desert conditions.

8. Reproduction of reptiles

Fertilization has become internal, and in all modern reptiles except
Sphenodon special organs of copulation derived from the cloacal wall
are developed in the male. In crocodiles and tortoises there is a single
median penis, but in lizards and snakes there are a pair of these struc-
tures, though only one is inserted at a time. The mechanism of erec-
tion involves both muscular action and vascular engorgement. The
sperms pass from the vasa deferentia into the urodaeum, and after

xiv. 8 REPRODUCTION 381

traversing this region they are carried into a groove along each penis.
In snakes the sperms may survive within the female for long periods,
and instances are known of isolated individuals laying fertile eggs
after months, sometimes even years, in captivity.

Some of the most serious difficulties in the colonization of the land
are concerned with reproduction, and these problems have been
largely solved in the reptiles, allowing the animals to reproduce with-
out returning, as many amphibia must do, to the water.

The eggs of oviparous reptiles are always laid on land. They there-
fore require a firm physical support and protection against desic-
cation, as well as an adequate supply of food and special means of
gaseous exchange and storage of waste products. These requirements
are met by the development of a shell, secreted by the walls of the
oviduct and often hardened by lime impregnation, by the formation
of special embryonic membranes, the amnion and allantois, and by
the provision of a large quantity of yolk enclosed in a bag, the yolk-
sac. The method of embryonic cleavage is affected by the great
amount of yolk, and as in birds is only partial. An albumen or egg-
white layer is present in the eggs of crocodiles and tortoises and pre-
sumably serves as a reservoir of water; in the eggs of lizards and
snakes, however, the albuminous layer is poorly developed or absent.

The formation of the amnion and allantois is one of the most
remarkable features of the development of reptiles ; it is characteristic
of all higher vertebrates, distinguishing them sharply from the lower
types. The amnion is developed from folds, which cover the embryo
and enclose a sac filled with fluid, where development can proceed
in the absence of the pond that was necessary for the earlier verte-
brates. The allantois began as an enlarged bladder, serving for the
reception of the waste products during the life within the shell. Coming
close to the surface and fusing with the chorion, it then becomes the
vehicle for the transport of oxygen to the embryo.

The evolution of eggs and embryonic membranes of the kind de-
scribed must have been an event of critical importance in tetrapod
history. Romer has suggested that this advance took place under
climatic conditions of alternate drought and flooding, so that eggs
laid above the high-water mark had the best chance of survival. Since
many of the early reptiles are thought to have spent much of their
time in the water, it is possible that the egg preceded the adult in the
process of adaptation to terrestrial life.

Most reptiles lay their eggs, but in many lizards and snakes these
are retained within the oviduct until the young are ready or nearly

382 REPTILES xiv. 8-

ready to hatch (e.g. Lacerta vivipara, Anguis fragilis, Vipera berus).
This method of reproduction is termed ovoviviparous ; in forms that
practise it the eggshell is reduced to a thin membrane or is lost
altogether. In some species (e.g. certain skinks and other lizards,
sea-snakes) a placenta is developed from the chorio-allantois or the
yolk-sac or both. The placenta may, as in Lacerta vivipara, serve only
for the transfer of water and gases, but in the more advanced forms it
probably provides a means of transport for food (supplementing the
yolk) and excretory products.

Young born alive are perhaps less susceptible to the hazards of
weather than those left to hatch in the sun or among rotting vegeta-
tion, and it is interesting that most, if not all, of the few reptiles that
live in places where the climate is really severe are ovoviviparous.

Young reptiles have special devices to assist their escape from the
egg. In Sphenodon, Chelonia, and Crocodilia, as in birds, there is a
horny epidermal egg-breaker on top of the snout tip, called the egg-
caruncle. In the Squamata, a true egg-tooth, projecting from the front
of the upper jaw, has the same function. The egg-tooth is present,
though sometimes rudimentary, in ovoviviparous forms.

Some reptiles make a simple nest but the group is not noted for
maternal care, usually abandoning their new-laid eggs or newborn
young. There are, however, some exceptions to this; female pythons
and certain other snakes and lizards brood their eggs, and female
alligators are said to guard their nests.

Many reptiles exhibit well-marked courtship and display pheno-
mena during the breeding-season, the males fighting and displaying,
either to intimidate each other or to evoke a suitable response from
the female. This is particularly striking in certain lizards, notably
those of the iguanid and agamid groups, where the males are often
brightly coloured and may be adorned with crests and distensible fans
under the throat. In these lizards bobbing movements of the head
and front part of the body, often accompanied by colour change, form
an important part of the display. As in birds, courtship may be associ-
ated with territory, a male holding an area of ground on which females,
but not rival males, are tolerated. Breeding behaviour and sexual
coloration are, of course, under the control of the endocrine system,
especially the anterior pituitary and the gonads, and may be modified
by castration. The onset of the breeding season is also influenced by
climatic conditions; most reptiles breed only once or twice a year,
but a few species living in warm stable climates may breed at intervals
nearly all the year round.

XIV. 9 (3 8 3)

9. Nervous system and receptors of reptiles

All the modifications of structure that fit the reptiles for life on
land would be useless without the development of appropriate be-
haviour. This in turn depends on suitable structure and function of

cer.h.

cLf.b.

<?** warn

hypoth.

Fig. 216. Three views of the brain of a lizard.

cereb. cerebellum; cer.h. cerebral hemispheres; hypoph. hypophysis;

hypoth. hypothalamus; olf.b. olfactory bulb; tect.opt. tectum opticum;

II— XII, cranial nerves. (After Frederikse.)

the nervous system. The brain accordingly shows some interesting
developments. The cerebral hemispheres are relatively larger in
reptiles than in amphibians (Fig. 216). The increased bulk lies mainly
in the basal parts of the hemisphere (the corpus striatum), as in birds
(Fig. 217). The roof (pallium) is little developed and lacks the elabor-
ate cortical differentiation found in mammals. The thalamus is well
developed and receives connexions from the optic tracts, which no
longer run mainly to the midbrain. There are also many fibres from the
thalamus to the cerebral hemispheres. This, together with the other
features mentioned, may be evidence for the transfer of many nervous

384 REPTILES xiv. 9

functions from lower levels of the nervous system to the cerebral
hemispheres, a process that has been carried much farther in mam-
mals. In most respects, however, the brains of modern reptiles are
more like those of birds than of mammals.

The behaviour of reptiles, despite the elaborate courtship of some
forms, remains of a relatively stereotyped character. The eyes are
usually the main exteroceptive sense-organs and are usually provided

co it dors.

cort. hipp.
sutc Llm

cert Cat

.ircfnstr

■palaeostr

Fig. 217. Transverse section through forebrain of Lacerta.

archistr. archistriatum (upper part of corpus striatum); cort. dors, dorsal cortex; cort. hipp.
medial (hippocampal) cortex; cort.lat. lateral (pyriform) cortex; palaeostr. paleostriatum
(basal part of corpus striatum); sept, septum; sidclim. sulcus limitans. (After de Lange

and Kappers.)

with movable eyelids, including a third eyelid or nictitating membrane.
The lacrymal and Harderian glands provide secretions that keep the
surface of the cornea moist. The eye is supported in most reptiles by
a scleral cartilage and a ring of bony scleral plates. Accommodation is
produced by the striated ciliary muscles, so arranged that they cause
the ciliary process to squeeze the lens, making its anterior surface more
rounded (Fig. 218). In many reptiles the retina possesses both rods
and cones, the latter predominating in diurnal types.

The pineal complex is often well developed, and in Sphenodon and
many lizards a 'pineal' or parietal eye is present with lens-like and
retina-like components. In such forms there is a pineal foramen in
the parietal bone near the fronto-parietal suture. Similar foramina
are found in many fossil reptiles, especially the more primitive types.
The function of the reptilian pineal is still rather obscure, but there
is evidence that in lizards it registers solar radiations, and, perhaps
by the secretion of hormones, influences the animal's thermoregula-

xiv. g

RECEPTOR ORGANS

385

tory behaviour in exposing itself to sunlight. It is also possible that the
pineal complex plays some part in the control of reproduction.

In the majority of reptiles the olfactory region of the nose is quite
well developed, but, except in crocodiles, there is only a single nasal
concha. The organ of Jacobson (vomero-nasal organ), a specialized
and sometimes separate region of the nose, innervated by a separate

THIS SIDE,
RELAXATION

THIS SIDE,
ACCOMMODATION

Fig. 218. Diagram to show the mechanism of accommodation in the eye of

reptiles.

ap. annular pad of lens; bm. Brucke's muscle; bp. base plate of ciliary body; c. cornea; ch.
chorioid; cp. ciliary process; 1. iris; lb. lens body; ot. ora terminalis; pi. pectinate ligament;
s.s. sclera; sc. scleral cartilage; scs. sclerocorneal sulcus; so. scleral ossicle; sr. sensory retina;
tbm. tendon of Brucke's muscle (continuous with inner layers of corneal substantia propria);
//. tenacular ligament; z. zonule. (From Walls, The Vertebrate Eye.)

branch of the olfactory nerve, is present in turtles, Sphenodon, and
Squamata. In the latter it is usually very highly developed (see
p. 405).

The tympanum when present lies at the back of the jaws, sunk a
little below the surface. The range of response to sound waves is not
known in lizards, but the ears of certain tortoises are very sensitive
to sound over a narrow range of about no cycles per second; appar-
ently there is some resonating mechanism, perhaps the columella auris,
which vibrates at this frequency. Generally speaking, the sense of
hearing is best developed among reptiles in the Crocodilia and certain
lizards.

EVOLUTION OF THE REPTILES

1. The earliest reptile populations, Anapsida

The organization of a reptile is well suited to maintain life on land.
Many features show a considerable advance in this respect over the
amphibia, for example, the dryness of the skin, the method of repro-
duction, and the devices for economizing in the use of water. The
immense radiation of the reptiles into every sort of land habitat during
the Mesozoic period shows the efficiency of these mechanisms, which
were probably present, at least in imperfect form, in the earliest Car-
boniferous and Permian offshoots from the ancestral Stegocephali

(P- 356).

We have sufficient knowledge to be able to trace the early stages of
reptilian evolution with considerable certainty. An animal known as
*Seymonria i found in the lower Permian of Texas (perhaps 250 million
years old), is of critical importance in our understanding of reptile
origins (Figs. 219, 220). It was a lizard-like creature, about 2 ft long,
probably living on insects and perhaps some larger animals. Its charac-
teristics are so exactly intermediate between those of amphibians and
reptiles that it is not possible to place it definitely with either group ;
many zoologists class it with the Amphibia. This intermediacy is
shown in almost every structure of the body and is often a subtle
matter of the shape or size of the parts. Although a list of anatomical
features is apt to give an unreal picture of any living organization it is
the only method available to us in the absence of any more ingenious
calculus, and we may therefore give first some of the characteristically
reptilian features of *Seymouria. (1) The neural arches of the verte-
brae were convex dorsally so that they have a 'swollen' appearance
which is also seen in early reptiles; (2) a canal for the lachrymal duct
was present; (3) the occipital condyle was single; (4) the pectoral
girdle possessed a long interclavicle; (5) the pelvic girdle was attached
to the vertebral column by two sacral vertebrae ; (6) the blade of the
ilium was expanded for the attachment of the large muscles used in
walking; (7) there were five digits in the hand instead of four as in
many labyrinthodonts and in living amphibia; (8) the phalangeal
formula was 2:3:4:5:3 or 4, approximating to the reptilian, rather
than the usual labyrinthodont condition, in which the phalanges are
less numerous.

Fig. 219. Skeleton of Seymouria. Actual length 20 in.
(From Williston, Osteology of the Reptiles, Harvard University Press.)

Fig. 220. Skull and pectoral girdle of Seymouria (after Williston).

c. coracoid; cl. clavicle; id. interclaviclc; j. jugal; /. lachrymal; m.
maxilla; po. post-orbital; qj. quadratojugal; sc. scapula; sq. squamosal.

xv. i SEYMOURIA 389

On the other hand, there are many considerations that would lead
one to classify this fossil as an amphibian. (1) The skull bones were
conspicuously pitted or 'sculptured' ; (2) the pattern of the bones was
very like that of early amphibians ; for instance an intertemporal bone
was present; (3) the teeth still showed a labyrinthine structure and
the palatal teeth were distributed in pairs as in many labyrinthodonts ;
(4) the structure of the otic notch, across which the tympanic mem-
brane was stretched, and certain other features of the auditory appara-
tus suggest amphibian rather than reptilian affinities; (5) other fossils
are known which, though clearly related to *Seymouria, show trends
such as flattening and reduced ossification of the skull that are charac-
teristic of late labyrinthodonts rather than early reptiles; (6) perhaps
the most significant point of all is that some adult specimens show
signs of the presence of lateral line canals. Since the structure of the
skeleton of *Seymouria suggests terrestrial habits, the presence of
these canals suggests that the animal may have passed through an
aquatic larval stage in which they were functional. Hence the case for
classifying * Seymouria as an amphibian becomes very strong.

It must be added that * Seymouria may show other features charac-
teristic of both early amphibians and primitive reptiles. The neck,
for example, was short, with the pectoral girdle lying close behind the
skull. There was little differentiation between the vertebrae, all those
in the cervical region bore ribs. The ribs were double-headed, a
feature that has been retained by some more advanced reptiles.

*Seymouria itself existed too late to have been a direct ancestor of
the more advanced groups of reptiles, since some of the latter had
already appeared by the early Permian. Whether it should actually
be classified as an amphibian or a reptile is uncertain; in Romer's
recent Osteology of the Reptiles it and its allies are placed in the latter
group. It may be regarded as a most interesting link between the
labyrinthodonts and the primitive stem-reptiles (Cotylosauria), from
which soon arose a great variety of descendants, which came to
dominate not only the land but also the sea and air throughout the
subsequent Mesozoic period.

The cotylosaurs must have existed throughout the later part of the
Carboniferous, though they did not become prominent before the
beginning of the Permian. From the Red Beds of Texas we have,
besides ^Seymouria, forms such as *Limnoscclis, *Captorhinus y and
*Labidosaurus, all with the rather high narrow skulls and pointed nose
characteristic of reptiles rather than amphibians, but differing from
the latter in the absence of the otic notch. This and other features

39Q

REPTILES

suggest that these animals were related to the early mammal-like rep-
tiles (p. 539). *Limnoscelis, however, was a particularly primitive form,
and may have been partly aquatic in habits.

Other rather later cotylosaurs were larger forms, such as *Diadectes
(Fig. 222) and *Bradysaunis and other 'pareiasaurs' from the Permian
and Triassic of Europe, Africa, and America. These were up to 10 ft

Limnosce'is

Captorhinus

Labidosaurus

Diadectes

Triassochelys

Bradysaurus
Fig. 222. Skulls of various early reptiles. After Romer and various authors.

long and probably carried the body well off the ground, the limbs
being held underneath the body and showing some reduction of
specialized digits. This, together with the large size of the animals and
their specialized teeth, suggest that they may have been one of the
first of the many types of large herbivore to appear on the land (see
p. 429). In some of them the skull developed grotesque protective
protuberances, a feature recalling similar later developments in
reptiles (Ceratopsia, p. 426) and mammals (amblypods, p. 717). A
characteristic structural feature was the presence of an otic notch low
down on the side of the skull. This distinguishes the pareiasaurs from
the more mammal-like forms and suggests affinity with some of the
other reptilian descendants of the early cotylosaurs. These cotylo-
saurs multiplied and became very diversified throughout the 45 million

XV. 2

CLASSIFICATION

39i

years of the Permian period, by which time the main reptilian types
had appeared. The individual reptilian orders nearly all became
established during the subsequent 45 million years of the Trias and
most of them reached their maximum development in the Jurassic
and Cretaceous.

2. Classification of reptiles

Since our knowledge of reptiles depends mainly on fossil remains
it is convenient to classify them by means of the skull into four great

Psrapsida

Diapsida

Fig. 223. Diagrams of reptilian skulls to show arrangement of the temporal openings.

Anapsida, no opening. Synapsida, a lower opening, with post-orbital and squamosal

meeting above it. Parapsida, an upper opening with post-orbital and squamosal

meeting below it. Diapsida, two openings, separated by a bar.

.jugal; pa. parietal; po. post-orbital; sq. squamosal. (From Romer, Vertebrate Paleontology,
Chicago University Press.)

groups (Fig. 223). Such a classification is in some ways artificial, but
it serves to indicate in a broad way the main lines of evolution within
the class.

In the cotylosaurs the dermal bones of the temporal region of the
skull presented an unbroken surface and there were no temporal
fossae. There were therefore no arches or 'apses' of bone in the tem-
poral region. Such forms are placed in the subclass Anapsida. The
jaw muscles took origin from the deep surface of the temporal side
wall, between it and the brain-case, and they passed down through
holes in the palate to be inserted on the lower jaw. This represents the
most primitive condition found in reptiles, and resembles that in the
early amphibians. It is still seen today, though often in a modified
form, in the Chelonia, which are hence placed in the anapsid sub-
class.

In more advanced groups of reptiles fossae bounded by bony
arches appear in the temple region, enabling the jaw muscles to extend

392 REPTILES xv. 2-

through them on to the outer surface of the skull, an arrangement
that increases their mechanical advantage.

In many reptiles, two such fossae appeared, the condition being
termed diapsid. This is seen in the subclasses Lepidosauria and Archo-
sauria, perhaps the most successful groups of reptiles. In lepidosaurs
of the order Squamata, however, the lower temporal arch is always
incomplete, having no quadrato-jugal bone and the jugal separated
from the squamosal. In some lizards and in snakes the upper arch
is also lost.

In other groups only a single fossa and arch is present. When this
is situated high on the skull the condition is known as parapsid.
Parapsid skulls are seen in the subclasses Ichthyopterygia (icthyo-
saurs) and Synaptosauria (plesiosaurs, &c). Formerly, these two sub-
classes were placed together in a group known as the Parapsida, as is
shown in Fig. 221, but this classification is now regarded as artificial,
since the ichthyosaurs and sauropterygians are not closely related;
in fact a careful analysis shows that the bony relationships of their
single temporal fossae were rather different.

In the remaining subclass, the Synapsida, there is also a single
fossa, but in the earlier forms at least it is placed low down, and is
bounded below by the jugal and squamosal. The term synapsid,
meaning 'fused arch', is actually a misnomer, due to the fact that
early workers believed, wrongly, that the single arch was formed from
the fusion of the two seen in diapsids.

The synapsids comprise the mammal-like reptiles, but in the later
members of the group, such as *Cynognathas, and in their descendants
the mammals, the temporal fossa has greatly enlarged, and has lost
its primitive relationships.

3. Order 1. Chelonia

Shut away in their boxes the tortoises and turtles have retained
some of the features of the earliest anapsid reptiles. Even today they
are a not unsuccessful and quite varied and widespread group, with
more than 200 species. These include terrestrial animals, such as
Testudo graeca, the Grecian tortoise of south Europe, which is her-
bivorous; the freshwater tortoises, such as Chrysemys and other
American terrapins, and Emys the European water-tortoise, all of
which are carnivorous. The marine Chelonia, usually known as
turtles, are often very large. Dermochelys, the leathery turtle, which
has no horny shell, is over 6 ft long and weighs half a ton. Chelone
my das, the green or edible turtle, is over 3 ft long.

xv. 3

CHELONIANS

393

The characteristic of chelonian organization is the shortening and
broadening of the body, together with the development of bony
plates, forming a box into which the head and limbs can be with-
drawn. The total number of segments is only about 8 in the neck, io
in the trunk, and a series of reduced caudals; the body is therefore

Fig. 224. Skeleton of turtle (Chelone).

carp, carpus (note hook-shaped 5th metacarpal); cen. centrum of vertebra; cor. coracoid;
fern, femur ;fib. fibula; h. humerus; il. ilium; isch. ischium; mar. marginal plate; nuch. nucal
plate; pr. 'proscapular' process or acromion; pub. pubis; rad. radius; rib, rib, partly fused
with costal shell-plate; sc. scapula (foreshortened); tib. tibia; uhi. ulna. (After Shipley and

McBride and Reynolds.)

morphologically shorter than in any other vertebrate except the frog.
Probably this shortening and broadening is the result of some quite
simple change in morphogenesis.

The shell is usually considered to include a dorsal carapace and
ventral plastron. Each of these is made up of inner plates of bone,
covered by separate outer plates of horny material, comparable to the
scales of other reptiles. The carapace includes five rows of bony plates,
namely, median neurals, and paired costals and marginals (Fig. 225).
These plates are ossifications in the dermis, attached to the vertebrae

394 REPTILES xv. 3

and ribs, but not actually formed from the latter. The plastron is
developed from the expanded dermal bones of the pectoral girdle,
together with dermal ossifications comparable to the abdominal ribs
found in crocodiles and other reptiles. The whole is covered in most
chelonians by rows of special smooth epidermal plates forming the
'tortoise shell' (Fig. 225). A new and larger layer is added to each of
these plates each year, the old one remaining above it, thus making a
number of 'growth rings' from which some indication of the age of the

Neur. S.

Neur. PL.

Mar (j. S.

Pect. S.

Fig. 225. Diagram of the arrangement of the shell of the tortoise

(Testudo). The horny shields are shown only on the left.

cap. capitulum of rib; cost.pl. costal plate; cost.s. costal shield; 7tiarg.pl. marginal

plate; marg.s. marginal shield; ncur.pl. neural plate; tieur.s. neural shield; pect.s.

pectoral shield; plast. plastron; sp.c. spinal cord. (After Gadow).

tortoise can be calculated, though the outer members often become
rubbed off.

In order to support this box the limb girdles have become much
modified and lie inside the encircling ribs. The pectoral girdle has
three prongs, a scapula that meets the carapace dorsally and carries a
long 'acromial process' and a backwardly directed coracoid, the two
last being attached bv ligaments to the plastron. The ilia are attached
to two sacral vertebrae and the ischia and pubis are broad. The limbs
are stout, but otherwise typically reptilian, with five digits in each.
In the marine turtles they are transformed into paddles.

The interpretation of the skull is still somewhat doubtful, but it
seems not unlikely that the turtle, Cheloue, shows the simplest case,
namely, the original anapsid condition (Fig. 226). Here the roofing is
complete, the dermal bones being widely separated from the brain-
case, forming a tunnel for the jaw muscles and those producing
retraction of the neck. The tympanum is stretched across a sort of otic
notch, bounded by the squamosal, quadrato-jugal and quadrate, the

xv. 3 SKULL 395

columella auris articulating with the latter. In other groups of Che-
Ionia, however, the dermal roofing has been reduced or 'emarginated',
presumably to give still better attachment for the jaw and neck muscles

Chelone

Trionyx

Fig. 226. Skulls of Chelone and Trionyx. Lettering as Fig. 214, p. 377.
(After Goodrich from Parker and Haswell, and Zittel.)

(Fig. 226). It has been argued that the condition in Chelone is second-
ary, but there is no evidence of true temporal fossae in any chelonian,
and since the early form *Triassochelys also had a fully roofed skull
there seems no reason for denying that we have here essentially an
anapsid condition.

A peculiarity of recent Chelonia is the entire absence of teeth, alike

(396)

Testudo

Fig. 227. Various chelonians, not all to same scale. (Emys and Chelys after Gadow,
Dermochelys after Deraniyagala.)

xv. 3 EGGS OF CHELONIA 397

in the herbivorous and carnivorous forms. The edges of the jaws form
sharp ridges, covered with a formidable horny beak.

The similarity of the soft parts of Chelonia to those of other
surviving reptiles (which are all diapsids) suggests that the
general organization of the group has changed little since the Per-
mian. The heart possesses a partly divided ventricle and there are two
equal aortic arches (Fig. 244). Respiration is modified by the rigidity
of the body wall; the lungs are spongy structures attached to the
dorsal surface of the shell, sometimes enclosed in a separate pleural
cavity (Testudo). Breathing is mainly brought about by the contraction
of the modified abdominal muscles, which function in a manner
comparable with that of the mammalian diaphragm, and by means of
pumping movements of the pharynx. Some aquatic forms {Emys) also
respire by taking water into special vascular sacs, diverticuli of the
urodaeum. The metabolism of tortoises is slow and they can remain
for long periods without breathing. In temperate climates all species
hibernate regularly.

The kidney is metanephric and the nitrogenous excreta are mainly
uric acid, there being a typical subdivision of the cloaca and reabsorp-
tion of water to form a solid whitish excretory product (see p. 380).
There is a single copulatory organ and the eggs are whitish, with hard
or soft shells. Like other aquatic reptiles that lay eggs, turtles all come
ashore to breed. Thus the marine Chelone breeds in the West Indies,
in the Straits of Malacca, and on the coast of West Africa; they are
caught as they come ashore and made into turtle soup. On the Amazon
chelonian eggs are (or at least were) so plentiful that large numbers
were eaten. The eggs are usually carefully placed in holes made by
boring with the tail and scooping with the feet (Emys). The traces of
the nest are then covered, often with considerable success. Neverthe-
less Bates reckoned that at least 48 million eggs were taken annually
on the upper Amazon. The chief enemies of the young are vultures
and alligators, and these were presumably the ultimate losers when
collection by man began, though the numbers of turtles have also
decreased as a result of the human depredations.

The proverbial slowness of the tortoise is a necessary corollary of
its heavy armour, but the nervous organization and behaviour is more
complex than is sometimes supposed. The brain shows well-developed
cerebral hemispheres, with not only the basal regions but also the
pallium quite large. This was therefore probably true also of the
earliest reptiles, as it is of amphibians. In the mammals, also derived
from cotylosaur ancestors, there has been still further development of

398 REPTILES xv. 3-

the dorsal regions of the hemispheres to form the cerebral cortex,
whereas in the remaining reptile groups, and in the birds, the ventral
portion has become large, the dorsal thin. The eyes are probably the
chief receptors of chelonians, but the nose is also well developed and
the animals are very sensitive to vibration. The tympanum is often
covered with ordinary skin and hearing is probably not acute (p. 385).
The voice is also small.

The various species show many special habits, some of them com-
plicated and ingenious, especially among the aquatic forms (Fig. 227).
For instance, the snapping turtles (Chelydra) and alligator turtles
(Macroclemys) of North America and Emys in Europe show con-
siderable care and skill in stalking and capturing not only fish but
also young ducks and other birds. Similarly the smaller turtles, such
as Chrysemys picta, the painted terrapin, with bright yellow, black,
and red colours, feed not only on insect larvae, but also on flies, which
they catch near the water surface. Many observers have shown that
the common Grecian tortoise has a marked sense of locality, returning
to a favourite spot even after hibernation.

Our knowledge of the geological history of the Chelonia extends
back to the Trias. *Triassochclys (Fig. 222) was an early turtle, with
a shell like that of modern forms, but still possessing teeth on the
palate. The skull was anapsid and the pectoral girdle contained inter-
clavicles, clavicles, and perhaps cleithra; these dermal bones were
already somewhat enlarged and incorporated in the plastron. The
head, tail, and limbs could not be withdrawn into the shell and were
protected by spines. In the later evolution of the Chelonia retraction
of the head became possible by one of two methods. In the suborder
Pleurodira, 'side-neck turtles', the neck is folded sideways. The group
is known from the Cretaceous and survives today in tropical Africa
(Chelys), South America, and Australia. The more successful group
is the suborder Cryptodira, in which the neck is curved in a dorso-
ventral plane. This type is also known from the Cretaceous and
includes most of the modern types. The aquatic chelonians show
various modifications and it is probable that several lines have inde-
pendently returned to the water. As a result of this habit the bony
shell is often reduced, presumably in the interests of lightness and
because of absence of enemies. This had occurred already in *Archelon
of the Cretaceous, which is very similar to the modern Chelone.
Dcrmochclys, the leathery turtle, has a curious 'carapace' consisting
only of a mosaic of small bony plates beneath its leathery skin,
and Trionyx is a freshwater turtle with a soft shell and no horny

xv. 4 SYNAPTOSAURS 399

plates. All of these forms are best considered as aberrant crypto-
dirans.

We can trace the history of the Chelonia back rather satisfactorily
to the Triassic, but unfortunately there is little to show how they
evolved to that stage from some Carboniferous cotylosaurian ances-
tor. * Eunotosaurus from the Permian of South Africa had a small
number of vertebrae, with very broad, expanded ribs. This perhaps
suggests some affinity with Chelonia, though in the latter the ribs
themselves are not expanded. There is therefore little to tell us how,
when, or why one of the early reptilian populations shortened its
bodies and covered them with armour for protection against the
hazards of the land they had recently invaded.

4. Subclass *Synaptosauria

Order *Protorosauria

All the Synaptosauria characteristically possessed a single temporal
fossa in the upper or parapsid position. The earliest forms were small
terrestrial lizard-like creatures such as *Araeoscelis from the lower
Permian (Fig. 228). A few more specialized forms, including the
remarkable Triassic * T any stropheus with, a long neck and short body,
are known, but the protorosaurs seem never to have been an impor-
tant element of the early reptilian fauna. Their relationships are not
well understood but it is possible that they gave rise to the sauro-
pterygians. The theory that the Squamata were derived from proto-
rosaurs by the emargination of the lower temporal region is now held
to be unlikely.

Order * Saw o pterygia

This was a very successful line of marine reptiles, extending from
the Trias to the end of the Cretaceous. The earlier nothosaurs, such as
*Lariosaurus (Fig. 228) from marine Triassic deposits, were small
(3 ft long) and had a long neck, and limbs partly converted into
paddles. The upper temporal fossa was enlarged and the nostrils lay
rather far back, as in many water reptiles.

All of these features were further developed in the plesiosaurs of
the Jurassic and Cretaceous, such as *Miiraenosaurns (Fig. 228). In
some the neck became very long, presumably for catching fish; 76 cer-
vical vertebrae have been recorded. In others the neck was shorter
and the skull longer. The limbs were developed into huge paddles,
the ventral portions of the girdles being large for the attachment of
muscle masses inserted on the flattened humerus and femur. The

400

REPTILES

xv. 4-

dorsal portion of the girdles, so well developed in terrestrial reptiles,
was here small: the ilium hardly articulates with the sacral verte-
brae. The hands and feet were enlarged by increase in number of
joints (hyperphalangy), but there was no increase of digits (hyper-

^^ammssk

-.-E»

Lariosaurus

^^^Mmmrn^ ^

Muraenosaurus

Ichthyosaurus \ Jf

Fig. 228. Icthyosaurs, plesiosaurs, and their allies. (Partly after Romer.)

dactyly) such as is seen in ichthyosaurs. The skull was as in notho-
saurs, but with the nostril still further displaced on to the upper
surface.

These animals were numerous in Jurassic and Cretaceous seas and
some of them reached 50 ft in length. They were obviously fish-
eaters, but little is known of their habits. It is not known whether they
were viviparous or came ashore to lay eggs. *Placodus and related

xv. 6 ICHTHYOSAURS 401

Triassic forms were related to the plesiosaurs and were specialized for
mollusc-eating by the development of large grinding teeth on the
jaws and palate.

5. Order *Ichthyopterygia

These animals, found mainly in the Triassic and Jurassic seas,
were even more modified for aquatic life than the plesiosaurs (Fig.
228). They occupied a position comparable to that of the dolphins
and whales during the Tertiary period. The body possessed a stream-
lined fish shape and swimming was by lateral undulatory movements.
The vertebrae were amphicoelous disks and there were large dorsal
and caudal fins, with the vertebral column apparently continued into
the lower lobe of the latter. The paired fins were small and presumably
used as stabilizing and steering agents. The pelvic girdle did not
articulate with the backbone. In the limbs the number of digits was
often greater or less than the usual five, and there was often hyper-
phalangy. Evidently this type of skeleton gives better support for a
fish-like paddle than does the pentadactyl tetrapod type and it is
interesting to find it evolved again in vertebrate stocks that returned
to the water. This seems in a sense to be a case of reversal of evolution.

The head was much modified for aquatic life, with a very long
snout armed with sharp teeth, and nostrils set far back. The eyes
were large and surrounded by a ring of sclerotic bony plates. The
temporal fossa, though in the parapsid position, had boundaries
different from that in the synaptosaurians.

The Triassic ichthyosaurs were already greatly modified and we
have no trace of the origin of the group. Romer has suggested a pos-
sible derivation from cotylosaurs related to the ancestors of mammal-
like reptiles. The ichthyosaurs were more highly adapted to aquatic
life than any other reptiles known. They seem to have been viviparous,
since the skeletons of small specimens have been found within larger
ones. Like the plesiosaurs they developed a special mollusc-eating
type, *Omphalosanriis, in the Triassic.

6. Subclass Lepidosauria

Most of the animals popularly considered as characteristic of the
period of reptilian dominance have a two-arched or diapsid skull. This
condition, or some modification of it, is found in all the surviving
reptiles except the Chelonia, and in the birds. Formerly all the two-
arched reptiles were placed in a single subclass, the Diapsida, but it
is now customary to divide them into two subclasses, the Lepidosauria,

402 REPTILES xv. 6-7

which includes Sphenodon, the lizards and snakes, and the Archo-
sauria, including the crocodiles, dinosaurs, pterosaurs, and the an-
cestors of birds. It is not known if the archosaurs were derived from
primitive lepidosaurs such as * Yonngina, or whether the two groups
arose independently from cotylosaurian ancestors.

Order *Eosuchia

The earliest lepidosaurs belong to the order Eosuchia. The best
known of these, * Youngina (Figs. 229 and 230), was a lizard-like
creature, found in the Upper Permian of South Africa, and retaining
many cotylosaurian features, for instance, teeth on the palate and no
opening between the bones of the snout (antorbital vacuity). The
two fossae at the back of the skull immediately show the affinity with
other diapsids. Little is known of the post-cranial skeleton. The fifth
metatarsal does not show the hooked shape that is found in other
diapsids and also in Chelonia. It is difficult, however, to ascribe very
great weight to this single point, as against the general features of the
skull, which indicate that * Youngina could have given rise to the later
two-arched reptiles and, by loss of the lower margin of the lower
temporal fossa, also to the lizards and snakes. *ProIacerta, from the
Lower Trias, shows how this may have come about; it is so like
* Youngina that it is classed as an eosuchian, but there is a gap in the
lower temporal arch, suggesting that the animal may have been near
the ancestry of lizards.

7. Order Rhynchocephalia

Sphenodon ( = Hatteria), the tuatara of New Zealand, is the oldest
surviving lepidosaurian reptile; it still remains in essentially the
eosuchian condition. Very similar Mesozoic fossils (e.g. *Homoeo-
saurus from the Jurassic) show the continuity of the type (Fig. 221).
Among the many primitive features that this race has preserved un-
changed for 200 million years are the two complete temporal fossae
(Fig. 231), the well-developed pineal eye (the pineal foramen is
marked in the early diapsid fossil skulls), and the amphicoelous verte-
brae with intercentra. Sphenodon, alone of surviving reptiles, has no
copulatory organ. The large wedge-shaped front teeth are among the
few specialized characters.

The tuatara was once widespread throughout New Zealand but
became much reduced and in danger of extinction. Recently rigid
conservation measures seem to have allowed it to recover in numbers
on some small northern islands. The animals are up to 2 feet long and

(4°3)

Fig. 229. Diagrams of skulls of A, eosuchian, B,
pseudosuchian, showing the plan of the diapsid skull.
Lettering as Fig. 214. //. lower temporal fossa; pi. pre-
orbital fossa; sf. upper temporal fossa. (From Goodrich.)

Fig 230 Skull of Youngina. Lettering as Fig. 214. (After Romer, Vertebrate Paleontology ,

Chicago University Press.)

4<h REPTILES xv. 7-

are insectivorous and carnivorous. They live in burrows, often in
association with petrels. The eggs take over a year to hatch.

Sphenodon evidently shows us a type that has departed relatively
little from the condition of diapsids in the late Permian. Yet its appear-
ance, habits, and soft parts are very like those of lizards, and provide
us with evidence that these animals remain in essentials rather close
to the original amniote populations. A few other extinct rhyncho-

itf. fr.

Fig. 231. Skull of Sphenodon. Lettering as Fig. 214. (After Romer,
Vertebrate Paleontology, Chicago University Press.)

cephalians are known; these include the rhynchosaurs, in which the
tip of the upper jaw had a hooked beak-like appearance.

8. Order Squamata

The lizards and snakes are the most successful of modern reptiles,
numbering between them over 5,000 species. Probably the groups
arose from eosuchians related to *Prolacerta. Such forms would also
have been close to the Rhynchocephalia, differing from them, however,
in a tendency to lose the lower temporal arch and to develop a movable
quadrate.

It has now been shown that the lizards are a more ancient group
than was formerly supposed, and had appeared by the end of the
Triassic. Furthermore, some of the early forms were already con-
siderably specialized. Our knowledge of the early lacertilian radiation
is still incomplete, however, and none of the existing lizard families
are known much before the Cretaceous. The earliest undoubted snake
occurs in the upper Cretaceous and the group does not seem to have
become abundant until the Oligocene.

xv. 8 LIZARDS AND SNAKES 405

Although typical lizards preserve a number of primitive reptilian
features, the Squamata as a group show several interesting specializa-
tions that are absent in Sphenodon, and to which their success may
be partly attributed. In the majority of forms, especially in the snakes,
the skull is highly kinetic, having a freely movable quadrate, which
imparts its motion to the bones of the upper jaw. Paired copulatory
organs of a unique type are present in the male. There is a widespread
tendency towards limb reduction, which has apparently occurred

Fig. 232. Jacobson's organ. Diagram of reconstructed L.S. of snout of lizard showing nose
and organ of Jacobson, both seen in section from the lateral side.

ex.n. region of external nostril; in. internal nostril; j.o. (/.) Jacobson's organ lumen ;/.o. (s.e.)
Jacobson's organ sensory epithelium; l.d. lachrymal duct, front end, cut; l.n. lining of nose;
n.j.o. nerves to Jacobson's organ; o.b. olfactory bulb; o.n. olfactory nerves; /. tongue.

independently in members of about half the existing families of
lizards, and in snakes.

The paired organs of Jacobson are highly elaborated and of great
functional importance. In snakes and in most lizards these organs
(Fig. 232) are hollow domed structures above the front of the palate,
each opening into the mouth by means of a slender duct. The lachry-
mal duct opens into or near the duct of Jacobson's organ, instead of
into the nose, suggesting that the secretions of the eye glands may have
some special function related to that of the organ. Odorous particles
are carried to the ducts of Jacobson's organs, or to the immediate
neighbourhood of them, by the tongue tip, which is forked in snakes
and many lizards. The lumen of the organ is partly lined by sensory
epithelium, supplied by a separate branch of the olfactory nerve.
Experiments by Noble and others have shown that the organs assist
in such functions as sex recognition and following trails left by prey.

(4o6)

*&m.

Sphenoaon /p^^f^i -^ ^- ;--<#

^§3&> "' -"^V,- r - . , • '* ... -/ A mphisbaena

Lyriocephalus

Fig. 233. Various Squamata {Draco after B.M. Guide).

xv. 8-9 LIZARDS 407

In some lizards and all snakes, the eyelids are modified to form an
immovable transparent spectacle covering the cornea, with the loss of
the nictitating membrane. The adaptive significance of this, which is
foreshadowed in some lizards by the development of a window in the
lower eyelid, is not always clear, since although it is found in many
that burrow or live in sand, it also occurs in arboreal forms.

9. Suborder Lacertilia

The modern lizards show extensive adaptive radiation (Fig. 233)
and include terrestrial, arboreal, burrowing, and aquatic forms. The
majority are carnivorous but there are some herbivores. It is difficult
to say which of the twenty or so living families is the most primitive,
and the grouping of these into infraorders is a matter of some difficulty.

The Gekkota contains the geckos and a small group of Australasian
limbless forms, the pygopodids. Geckos are mainly small nocturnal
and arboreal insectivorous lizards of warm climates, with ridged pads
on the toes and sharp claws that enable them to climb an almost
smooth surface. Some species have taken to living in houses. The
tree-gecko Ptychozoon has webs of skin on the limbs and along the
sides of the body, which perhaps act as a parachute to break its fall.
Many geckos live in colonies and unlike most lizards are extremely
vocal, making clicking and cheeping sounds. Their hearing is probably
acute. The endolymphatic ducts of the inner ear are greatly expanded
to form sacs in the neck containing calcareous deposits, but the func-
tional significance of this is obscure. Their eyes are, as a rule, covered
by a spectacle. Geckos are the only Squamata that lay hard-shelled
eggs, those of other forms being leathery in texture.

The Iguania is a large group comprising the agamids, iguanids, and
chameleons. The first two include terrestrial, arboreal, and amphibious
types, sometimes of large size, and often furnished with crests, dew-
laps, expansible throat-fans and other appendages that play a part
in rivalry and courtship. The males are often brightly coloured and
the whole group is characterized by a visually dominant behaviour
pattern. In some arboreal forms, as in the chameleons, the sensory
parts of the nose and the organ of Jacobson are reduced.

The agamids are found in the Old World and Australasia and in-
clude such well-known types as the oriental 'blood-sucker' (Calotes),
so-called because of the red colour of the throat, the spiny lizards
(Uromastix) of the north African and Indian deserts, and the Aus-
tralian frilled lizard (Chlamydosaarns) (Fig. 240). The Indo-Malayan
genus Draco has a large lateral web, supported by the ribs, which can

4o8 REPTILES xv. 9

be spread out and used for gliding, though it is not moved in true
flight. Lyriocephalus from Ceylon is an agamid with a remarkable
convergent similarity to the chameleons. Some agamids (and other

Fig. 234. Chameleon catching a fly, showing its changes in colour.

A, cream with yellow patches, the usual night colour. B, grey-green with
darker patches. C, dark brown patches and yellow spots. D, reaction pro-
duced by pinching tail, inflation and darkening of all spots. (After Gadow.)

lizards) can run on their hind legs when they are in a hurry (Fig. 240).
In agamids the teeth are set squarely on the summit of the jaw, as in
Sphenodon; this condition is termed acrodont. In most other lizards
the teeth are attached obliquely to the inner side of the jaw (pleuro-
dont).

The iguanids are found mainly in the New World and parallel the
agamids in many ways. Anolis is a small, common North American
form. Iguana from south and central America reaches 6 ft in length.

xv. 9 LIZARDS 409

Amblyrhynchus, found only in the Galapagos Islands, is remarkable
as the only existing marine lizard, though it spends much of its time
on shore, basking and feeding on the sea-weed left at high tide. Phryno-
soma, the horned toad, with spikes on the head and back, is found in
the deserts of North America and burrows in the sand. This is one of
the few ovoviviparous iguanids.

The chameleons are highly modified arboreal lizards from Africa,
Madagascar, and India. Some species have casques on the head, or
one or more horns on the snout. The tail is prehensile and the digits
are arranged in groups of two and three so as to be opposable and
allow the grasping of branches. Chameleons live on insects, caught
by means of the very long tongue (Fig. 234), which has an adhesive
clubbed tip and is projected by a remarkable muscular mechanism.
Their movements are slow and deliberate, but they show considerable
care in stalking their prey; as they approach it their eyes, which
normally move independently, converge so as to bring the prey into
binocular vision, presumably serving to judge its distance. Their
powers of colour change are described on p. 410.

The Scincomorpha are another large assemblage, including Lacerta,
common in Europe and North Africa, and the skinks, many of which
are modified for burrowing, sometimes in the sand. Many skinks
have well-developed limbs, but others show all degrees of limb reduc-
tion, either the fore- or hind-limbs, or both, being lost. The most
highly fossorial of all lizards, the worm-lizards or Amphisbaenidae,
may also belong to the Scincomorpha, though they show many
remarkable specializations. Their eyes are rudimentary, their tails are
blunt and resemble the head, and they are able to move freely in
either backward or forward direction. External limbs are usually
absent.

The Anguimorpha contains the anguids, of which the European
slow-worm Anguis is a familiar limbless example, and the monitor
lizards (Varanus) and their allies, which are placed in the superfamily
Platynota. The monitors of the Old World and Australia include the
largest of existing lizards, one species, the Komodo Dragon, growing
to at least 10 ft long. They are carnivorous, killing vertebrates as well
as insects, and are often semi-aquatic. Three related groups, now
extinct, occurred in the Cretaceous. The aigialosaurs and dolichosaurs
were amphibious lizards of moderate size, but the later mosasaurs,
such as *Tylosawus, were huge creatures, sometimes 30 ft long, and
were highly adapted for marine life, with long jaws and paddle-
like limbs showing some hypcrphalangy. The strikingly coloured

410 REPTILES xv. 9-

heloderms from North and Central America are also playtnotids and are
of special interest as the only known poisonous lizards. Another allied
form is the rare earless monitor, Lanthanotus, from Borneo, which
seems to be a survivor of the primitive platynotid stock.

Many lizards are able to change colour, the chameleons, Anolis
(often called 'American chameleons'), and certain agamids being the
most notable for this. The colour may change with the environment,
serving the obvious purpose of concealment. Special colour patterns

Fig. 235. Diagram of the nervous control of the melanophores in the chameleon
(above) and minnow (below).

c, spinal cord; f, pathway of pigmentomotor fibres (the synapse in the sympathetic ganglia

is omitted); M, melanophore; n, spinal nerve; p, pigmentomotor centre; s, sympathetic.

(From Sand, minnow after v. Frisch.)

are displayed in courtship or threat, and colour change may also
occur in response to temperature and other environmental changes.
The physiological mechanism of colour control varies in different
reptiles. In Anolis there are probably no nerves to the melanophores,
which are controlled by hormones produced by the posterior pituitary
and possibly other glands. In chameleons, however, the melanophores
are controlled partly or entirely by the autonomic nervous system
(Fig. 235).

Many lizards are able to break off their tails when threatened or
seized by a predator; this ability, known as autotomy, is due to the
presence of special planes of weakness through the bodies of the caudal
vertebrae. Such fracture planes are also found in Sphenodon, but not
in snakes. After autotomy the tail regenerates, but the new member
is not a replica of the normal. The vertebrae, for instance, are not
regenerated, their place being taken by an unsegmented tube of car-
tilage. It has been shown experimentally that in Anolis regeneration
will not occur if the motor-nerves are prevented from growing back

xv. io SNAKES 411

from the stump. The new sensory innervation of the skin is derived
entirely from the surviving dorsal roots, whose cells become greatly
enlarged.

10. Suborder Ophidia

The snakes are obviously descended from lizards of some kind, but
their precise mode of origin is obscure. Some workers believe that
their nearest living relatives are the platynotid lizards (monitors, &c).
There is evidence that the snakes passed through a burrowing stage in
their early history, although no known platynotids show marked fos-
sorial adaptation. A burrowing ancestry is particularly suggested by
the structure of the eye, which, as Walls has pointed out, differs
widely from that in typical lizards (Fig. 238). Thus there are no
scleral ossicles or cartilages in snakes, and accommodation is brought
about in a manner unusual for reptiles, involving displacement of the
lens. The visual cells include cones of a peculiar type, which have
apparently been derived from rods. The yellow retinal droplets that
serve to protect lacertilian retinae from excessive light are absent,
and instead some diurnal snakes protect their retinas by a yellow-
tinted lens. These features can all be interpreted on the supposition
that the ophidian eye was once drastically reduced, but has sub-
sequently been refurbished in response to the needs of life above
ground. Other characters that seem to point in the same direction
include the structure of the ears which, as in many burrowing lizards,
have apparently degenerated. The ear drums, tympanic cavities, and
Eustachian tubes are absent, and the columella auris articulates with
the quadrate. It seems unlikely that snakes can hear airborne sounds
at all well, though doubtless they are sensitive to ground vibrations
transmitted through the bones of the jaw.

The snakes show many other interesting peculiarities, the most
obvious being the complete absence of limbs. Only in a few of the
more primitive forms such as the boas and pythons can rudiments of
the hind limbs and their girdles be found; in these snakes claws may
be present externally on either side of the cloaca and are said to play
a part in coitus.

Locomotion is produced by the lateral undulation of the body,
which exerts pressure on surrounding objects and pushes the snake
forwards; the enlarged transverse ventral scales of most species help
to prevent slipping. A few snakes (e.g. some boas and vipers) can also
progress by muscular movements of the ventral scales, with their
bodies stretched out almost in a straight line. The spine is strengthened

4 i2 REPTILES xv. 10

by additional intervertebral articulations known as the zygantra and
zygosphenes.

The skull is highly modified, permitting, in all except a few bur-
rowing forms, an enormous gape and the swallowing whole of large
prey. The premaxilla is small and usually toothless, and the bones of
the upper jaw are loosely attached to the rest of the skull. The two
halves of the lower jaw are united only by ligaments. The sharp
recurved teeth are carried on the palate bones as well as on the maxilla

pro. / WSW5"
sm. pi.

Fig. 236. Diagram of skull in ophidians.
d. dentary; ec. ectopterygoid ; jr. frontal; mx. maxilla; ». nostril; na. nasal; 0. orbit; pa.
parietal; pf. postfrontal; pi. palatine; pm. premaxilla; prf. prefrontal; pt. pterygoid; q. quad-
rate; s. squamosal or supratemporal; sf. upper temporal fossa (this is shown diagram-
matically, as it occurs in many lizards; in Lacerta it is largely covered by an extension of
the postfrontal — see Fig. 213); sm. septomaxilla. (Modified from Goodrich.)

and dentary. The brain-case is strong and compact, the brain being
protected from mechanical injury during swallowing by the massive
parasphenoid and by flanges of the frontals and parietals, which lie
between the orbits, so that there is no interorbital septum.

In the normal ophidian kinetic mechanism the upper jaw as a whole
is raised as the result of forward rotation of the lower end of the freely
mobile quadrate, which is attached to the back of the pterygoid. The
well-developed protractor muscles of the pterygoid and quadrate play
an important part in the process. In the viperid snakes a further
elaboration of this mechanism is seen, the maxilla being very short
and able to rotate on the prefrontal so that the fangs can be erected
(Fig. 237). A slip from one of the muscles is attached to the poison
gland and helps to expel the venom as the snake bites.

The respiratory system and viscera of snakes are also much modi-
fled. The glottis can be protruded so as to keep the airway clear while
prey is being swallowed, and in some forms a part of the trachea is
specialized for respiration as a tracheal lung. The left of the two paired

XV. IO

SNAKES

4i3

lungs is usually reduced, often to a rudiment, as in some limbless
lizards, and the other paired viscera tend to lie at different levels on
the two sides. The heart usually lies a quarter to a third of the way
down the body, and the carotid arches are asymmetrical, the right
common carotid artery tending to be suppressed.

max

temp ant

Fig. 237. Skull of rattle-snake (Crotalus) with jaws partly and fully opened.

Lettering as Fig. 214; sph-pt. the protractor-pterygoid muscle, which pulls the pterygoid
forward, causing it to push the ectopterygoid, which rotates the maxilla and erects the
fang; di. the digastric muscle that assists in opening the jaw; temp. ant. the anterior temporal
which shuts the mouth. The diagrams at the right show the actions of the levers that erect
the fang; g is the groove characteristic of crotaline snakes. (Modified after Gadow.)

The snakes show nearly as much adaptive radiation as the lizards,
though there is less structural variation among them. The more pri-
mitive forms, with pelvic rudiments, include a number of small bur-
rowers such as Typhlops, as well as the large boas and pythons of the
family Boidae, which tend to be arboreal and amphibious in habits
and kill their prey by constriction. In general, the pythons lay eggs,
whereas the boas are ovoviviparous.

The majority of living snakes belong to the family Colubridae, which
contains many medium-sized harmless snakes such as the grass-snake
(Natrix) and some moderately poisonous ones with grooved fangs at

Ectodermal
sphincter, ci!at<

Base pi <.

Canal of Schlemm
'in sclera)
Ciliary processes
lacking

Scleral ossicle
■art/ muscle

■Sclera (cartilage)
'Choribid

'Retina (avascular
cone a! droplets and with standard
double cones)

Lizard

Spectacle

Mesodermal
sphincter, dilatator

raconjunctiysl space

Canal cf Schlemm
(in cornea)

No cone oil droplets

No epichoricidal lymph spaces

Mesodermal Afcht^S c ' er3 (™™4

Con us / // /y^Lhorioid

■Retina (with
unique double cones)

Snake

Fig. 238. Diagrams of eyes of lizard and snake, to show the marked contrasts

resulting from presumed loss during underground life and later acquisition by the

snakes of features paralleling those present in their ancestors. The dotted arrows

show the direction of application of force during accommodation.

(From Walls, The Vertebrate Eye.)

XV. IO

SNAKES

4i5

the back of the maxillae; these are known as back- fang snakes or
opisthoglyphs. The South African boomslang (Dispholidus) is one of
the few whose bite may be lethal in man. Dasypeltis, the egg-eating
snake, is also a member of this group ; it swallows the eggs whole and
crushes them with special tooth-like processes of the neck vertebrae.
The family Elapidae contains the cobras, kraits, and coral snakes,
all highly poisonous with quite small and relatively non-movable fangs
at the front of the maxilla, and a venom predominantly neuro-toxic in

<l'S tp

Fig. 239. Head of crotaline snake (Lachesis) after removal of skin.

d. duct of poison gland, bending at base of fang; dig. digastric muscle; g. sensory pit or

groove ; n. nostril ; p.g. poison gland ; ta. and tp. anterior and posterior portions of temporalis

muscle; tr. trachea. (From Gadow.)

action. All the poisonous Australian snakes belong to this group. The
hood of the cobra is expanded by the long cervical ribs and probably
has a warning (sematic) function. The king cobra (Hamadryas) is the
largest poisonous snake and reaches 18 feet in length.

The very poisonous sea-snakes (Hydrophiidae) are related to the
elapids. Their tails are vertically compressed for swimming; some
species can hardly move on land. Like many freshwater snakes they
are (with a few exceptions) ovoviviparous.

The family Viperidae consists of the vipers of the Old World and
the rattle-snakes and pit-vipers, mainly from the New World. The
two latter groups, placed in the subfamily Crotalinae, are distinguished
by the presence of a remarkable sensory pit on each side of the head
between eye and nostril (Fig. 239). This is highly sensitive to tem-
perature changes and helps the snake to detect warm-blooded prey.
The rattle-snakes are, of course, also noted for their caudal append-
ages, which are composed of articulated rings and modified skin. One
ring is formed at each moult, though the older and most posterior
ones break off periodically. The rattle is vibrated voluntarily as a

416 REPTILES xv. 10-

vvarning and perhaps prevents the snake from being trodden on by
large mammals.

Most of the Viperidae are highly poisonous, though the bite of the
European adder {Vipera berus) is seldom fatal to man. The venom is
predominantly haemolytic in action. The fangs are canalized, the
canal having apparently being evolved by the progressive deepening
of a groove until its margins have come into apposition. The fact
that the fangs are erected when the snake strikes and can be folded
back along the roof of the mouth when not in use, makes it possible

Fig. 240. Drawings of three frilled lizards (Chlamydosaurus) and a Grammatophora

(at right) to show the bipedal habit. (Drawings made by Heilmann from photographs

of the lizards running at full speed, taken by Saville Kent.)

for these structures to be very long, about 1 inch in the case of a large
puff adder.

Some of the American pit-vipers are very large, the dreaded bush-
master (Lachesis) reaching about 10 ft. The majority of the Viperidae
bear their young alive and the finding of late embryos within the
bodies of female adders and rattle-snakes may have given rise to the
tale and that these reptiles temporarily hide their young by swallowing
them in the face of danger.

1 1 . Superorder Archosauria

We have seen that about 130 million years ago the diapsid stock
produced the most successful modern reptile group, the Squamata
(Fig. 221). Much earlier an even more successful type had developed
from the Eosuchia, having as its outstanding feature the habit of walk-
ing on the hind legs. Creatures of this type were the dominant land
animals of the later Mesozoic, and they include the dinosaurs and
pterosaurs. Crocodiles are the only living descendants of the group

xv. i 3 ARCHOSAURS 417

that have remained at the reptilian level. They have, of course, aban-
doned the bipedal habit and survive as a specialized amphibious
remnant. The birds, which are also undoubtedly descendants of this
archosaurian group, give us in some ways a better idea of the charac-
teristic structure than do the crocodiles.

All the lines of archosaurs are characterized by certain common
tendencies, mostly associated with bipedalism, which is possible also
in some lizards (Fig. 240); features barely indicated in the earlier
forms become developed in the later. In all archosaurs the hind legs
were much longer than the front and the acetabulum formed a cup,
open below, so that the legs were held vertically below the body. At
the same time the ischium and pubis became elongated, presumably
to allow for the attachment of muscles producing a fore-and-aft move-
ment (see p. 375). In later forms the ilium became fused with several
sacral vertebrae. The femur has a lateral head and the tibia becomes
long and strong and sometimes fused with the proximal tarsals; the
distal tarsals may fuse with the metatarsals as in birds, and the digits
are reduced, usually to three long ones turned forward while the first
is turned back. The skull is typically diapsid, but tends to have cer-
tain modifications, such as the development of antorbital vacuities
behind the nostrils and other spaces in the palate, presumably serving
to give lightness without loss of strength.

12. Order *Pseudosuchia

The earliest archosaurs were the Triassic pseudosuchians, creatures
evidently not far removed from the Permian eosuchians. These
animals (*Saltoposuchus) can be visualized as lizards that ran on their
hind legs (Fig. 241). They were small and carnivorous, having sharp
teeth set in sockets along the edges of the jaws (hence 'thecodont').
The skeleton showed all the archosaur characters in a most interesting
incipient form. Thus the bones of the pelvis were still plate-like, but
arranged in the characteristic triradiate manner. The front legs were
already much shorter than the hind. Antorbital vacuities were present
and there was no pineal foramen.

13. Order *Phytosauria

Even in the Triassic at least one line, the phytosaurs, abandoned
the bipedal habit, becoming amphibious. These creatures were not
actually ancestral to the crocodiles, but show remarkable parallelism
to them in the elongated jaws and general build (Fig. 241). How-
ever the nostrils were set far back. There can be no doubt that the

418 REPTILES xv. 13-

phytosaurs were derived from pseudosuchians and the two groups are
often placed together in an order Thecodontia.

Compsognnthus

Fig. 241. The skeletons of various archosaurian diapsids.
(Modified after various authors.)

14. Order Crocodilia

In the crocodiles the nostrils are at the tip of the snout and the air
is carried back in a long tube, the maxillae, palatines, and pterygoids
forming a bony secondary palate, as in mammals. There is a flap on
the hind end of the tongue, which, with a fold of the palate, enables
the mouth to be closed off from the respiratory passage and hence
kept open under water. The nostrils can also be closed by a special

xv. 14

CROCODILES

419

set of muscles, and the ear-drums are protected by scaly movable
flaps. The Eustachian tubes are very complicated, and parts of the
skull are pneumatized by extensions from the middle ear cavity, as in
birds.

Fig. 242. Diagram of the skull of Crocodilia.
Lettering as Fig. 214, p. 377. (From Goodrich.)

Fig. 243. Anterior cervical vertebrae of Crocodilus.

c. capitulum; lip. hypocentrum; wa 1-4 , neural arches; pa. pro-atlas; pi. 1-4, pleurocentra;
prz. prezygapophysis; ptz. postzygapophysis; r. rib; t. tuberculum; tp. transverse process.
The first neural arch and the pro-atlas of the left side have been removed to show the first
pleuro-centrum (pi 1 ) which is the odontoid process. (From Goodrich.)

The crocodiles use all four limbs in walking, but the front are
shorter than the hind, indicating bipedal ancestry. The pelvis of the
crocodiles shows signs of the typical triradiate structure, but there
are only two sacral vertebrae. Rapid swimming is produced by lateral
movements of the tail, but when moving slowly the partly webbed
feet are used to push the animal along. The ribs (Fig. 243) are two-
headed and there is a proatlas element between the skull and atlas.
The scutes of the back and, in some forms, of the belly, are rein-
forced by osteoderms, and there are well-developed abdominal
ribs.

420

REPTILES

xv. 14-

The soft parts of the crocodiles are of special interest because croco-
diles are, except the birds, the only living creatures closely related to
the great group of dinosaurs. The heart (Fig. 245) shows a complete
division of the ventricle, but there are still two aortic arches. The
truncus arteriosus is divided in a spiral manner to its base, so that
the aortae cross and the right arch opens from the thick-walled left

car int.

car. cxt

car. int.

I 1 1 1 „ car. ext

v.c.
Che Ionian

Crocodile J

Fig. 244. Fig. 245.

Diagram of heart and arterial arches of a chelonian and of a crocodile, seen from below.
Lettering as Fig. 215, p. 379. (From Ihle, after Goodrich.)

ventricle, while the left opens with the pulmonary arteries from the
weaker right ventricle. The left arch would therefore contain venous
blood, but an aperture, the foramen of Panizza, connects the two
arches near the base and presumably the higher pressure in the left
ventricle ensures that the left arch receives at least some oxygenated
blood. Possibly, however, the pressure in the right ventricle is in-
creased when the crocodile dives and the blood flows through the
foramen from right to left.

The lungs are well developed, having a system of tubes ending in
sacs. A transverse partition separates off a thoracic from the main
abdominal cavity. This 'diaphragm' is not itself muscular, but is
continued into a diaphragmatic muscle attached to the abdominal
sternal plates. This muscle, innervated by abdominal spinal nerves,

xv. 15 DINOSAURS 421

presumably assists in respiration. It is a development for this purpose
quite distinct from the mammalian diaphragm. It is not impossible
that the dinosaurs possessed further developments of this arrangement
of the heart and lungs, and that they owed some of their success to
this mechanism.

The modern crocodiles represent only the survivors of a once much
more abundant group. Crocodilus is the most widespread genus,
occurring in Central America, Africa and Asia, Malay and East
Indies, and North Australia. Alligator, with each fourth lower tooth
penetrating into a hole in the maxilla, is found in North America and
in China. Caiman of Central and South America is related to Alligator.
The length of the snout varies considerably in different species, and
is extremely long and slender in the fish-eating Gavialis, Indian
gharial, and Tomistoma of the East Indies. Crocodiles lay hard-shelled
eggs in large clutches, depositing them in the sand or in nests com-
posed of vegetation. The crocodiles seem to have changed little since
they first appeared in the late Triassic, perhaps 190 million years ago.
*Protosuchns of that time had a pelvis like that of crocodiles but was
otherwise very like a pseudosuchian. There were numerous types of
crocodile in the Jurassic and Cretaceous, living both in fresh water
and in the sea. In these forms the palate was closed only as far back as
the palatine bones; the addition of flanges of the pterygoids took
place only in the Eocene crocodiles, which were numerous in many
parts of the world, including northern continental regions that today
are too cold for such animals. In spite of their specializations for
aquatic life, the crocodiles show us many features that were present
in the earliest archosaurs and they therefore give some idea of the
characteristics of the ancestors of the pterodactyls, dinosaurs,
and birds.

15. The 'Terrible Lizards', Dinosaurs

In the 10 million or so years at the end of the Triassic some of the
descendants of the pseudosuchians became very successful and numer-
ous and many of them were very large. The large size was not a
characteristic only of one line but of two quite distinct ones, each with
several sub-divisions. The term dinosaur is applied to all of them, but
the two main lines have little in common beyond the characters
common to all archosaurs. The desire to explain this extraordinary
exuberance of reptiles has attracted much attention to these
giants.

xv. 1 6

Fig. 246. The skeletons of various saurischian dinosaurs.
(Modified after various authors.)

16. Order *Saurischia

These include forms with a triradiate pelvis, very like that of the
pseudosuchians. The earlier types, like their ancestors, were bipedal
carnivores of no great size, such as *Compsognathus from the Jurassic

xv. 16 THEROPODS 423

of Europe and *Ornitholestes from that of North America (Fig. 241).
The front legs were short, with 4 or 3 digits, provided with claws ; the
pectoral girdle was reduced to scapula and small coracoid, with no
trace of clavicles. Some members of this line, the theropods, soon
developed into large carnivores, such as *Allosanrus (Fig. 246), over
30 ft long (Jurassic, North America). These animals apparently
swallowed their food whole and to help with this the quadrate was
movable and there was a joint between the frontals and parietals, as
in many lizards. In other respects the skull was very similar to that of
the pseudosuchians.

At the end of the Cretaceous this theropod line produced the largest
carnivores that have appeared on the earth, such as *Tyrannosaurus
rex, nearly 50 ft long and 20 ft high, from North America. All the
previously mentioned tendencies were here accentuated, producing
creatures with bipedal habit, very powerful head and jaws, and much-
reduced fore-limbs. They presumably preyed upon the large herbi-
vorous dinosaurs of the Cretaceous and became extinct with their
prey, either from a common inability to meet the rigours of the climate
or in competition with the mammals and birds. Throughout most
of the Jurassic and Cretaceous the theropods were the dominant
carnivores of the world, taking the place occupied earlier by the
synapsid reptiles (p. 540) and later again by descendants of the synap-
sids, the carnivorous mammals.

In the Cretaceous the organization of this saurischian line also
produced some exceedingly bird-like forms, *Struthiomimus and
*Ornitho)ithnus, walking on three toes and having three also in the
hand, one opposable and used for grasping. The skull became very
lightly built and the teeth disappeared, possibly in connexion with an
egg-eating habit (Fig. 246).

All these carnivorous, bipedal saurichians may be grouped into a
suborder Theropoda. Another line of organization, starting from
bipedal, carnivorous Triassic theropods, adopted a herbivorous diet
and reverted to the quadrupedal habit. These animals, the suborder
Sauropoda, culminated in the immense Jurassic forms, * Apatosaurus
(= *Brontosaurus) and *Diplodocus, the largest of all terrestrial
vertebrates. Several stages of the transition from bipedal to quad-
rupedal habit can be traced. * Yaleosaimis from the Trias was a bipedal
creature 6 ft long but with rather long front and short hind legs.
*Plateosaurns, also of the Trias, was 20 ft long, but still bipedal. Soon
the front limbs became larger and more used for walking, though the
disparity always remained. The neck was immensely elongated and

424 REPTILES xv. 16-

the head very small, with a lightly built skull. The nostrils lay on the
top of the head and in *Diplodocus formed a single opening. This
seems to indicate that the animals were aquatic or amphibious, as
would in any case be suspected from the very large size, making it
unlikely that the legs could bear the full weight. *Diplodocus and
*Brachiosaurns were over 80 ft long and the weight of the latter must
have been nearly 50 tons. However, the structure of the vertebral
column shows that much weight was carried on the legs, for the verte-
brae are strong, though hollowed in places. Footprints of the animals
have been found. One or more of the digits bore claws. The skull
became relatively short and broad, and among the many puzzling
features of these giant animals is the weakness of the jaws and small
size of the teeth, mostly crowded towards the front of the mouth.
These teeth would have served well enough for cropping, but there
are no teeth on the hind part of the jaws and no provision for grinding
the food. Animals of large size can only have been supported by this
feeble apparatus if some very nutritious food was readily available.
This perhaps agrees with the small size of the brain, which was
several times smaller than the lumbar enlargement of the cord.

17. Order *Ornithischia

The second main group of dinosaurs appeared later than the sauro-
pods and possessed a 4-radiate pelvis, with the pubis directed back-
wards and an extra pre-pubic bone pointing forwards. The teeth were
restricted to the hind part of the jaws, the front bearing a beak. At the
front end of the lower jaw there was an extra bone (predentary).
These were herbivorous forms and they appeared in the Jurassic and
achieved their maximum in the Cretaceous, by which time the sauro-
pods had become less common. The earliest of the ornithischians
were bipedal animals, included in a suborder Ornithopoda, from the
Jurassic and Cretaceous. These animals, such as *Iguanodon, were
built on the same general lines as the pseudosuchians, from which
they were presumably derived. The skull was heavily built and adapted
for a herbivorous diet, with powerful muscles attached to a coronoid
process of the lower jaw. The bipedalism was less marked than in
saurischians and the fore-limbs less reduced. Several separate lines
then reverted to a quadrupedal habit. The trachodonts (*Hadro-
saurus) were a very successful group of amphibious forms in the
Cretaceous, with webbed feet. The teeth were suited for grinding,
parallel rows being present, making as many as 2,000 teeth in one
animal. In several types of hadrosaur the top of the head was pro-

xv. i7

DINOSAURS

425

Triceratops

Fig. 247. The skeletons of various ornithischian dinosaurs.
(Modified after various authors.)

longed in various ways, giving a structure that perhaps allowed the
nostrils to remain above water while the animal was feeding below.
These animals reached 30 ft in length and may have supplanted the
sauropods as marsh-living forms, possibly when the soft foods gave
place to harder plants.

Other lines of ornithischians became more fully terrestrial and
quadrupedal and were mostly heavilv armoured. Thus the stegosaurs
of the Jurassic carried immense spines on the back and the tail bore

426 REPTILES xv. 17-

sharp spikes. The hind legs were much longer than the front, a relic of
bipedal ancestry. The feet carried hoof-like structures. The skull was
very small and the brain much smaller than the lumbar swelling of
the cord. The teeth were in a single row and small. The ankylosaurs
of the Cretaceous were covered all over with bony plates, somewhat
in the manner of the mammalian glyptodonts (*Nodosaurus, Fig. 247).
Finally, the ceratopsians, such as * Triceratops of the late Cretaceous,
developed enormous heads, with huge horns and a large bony frill,
formed by extension of the parietals and squamosals to cover the neck.
These later Cretaceous animals appear to have lived on dry land and to
have walked on all fours, although the bipedal ancestry is shown in
the shortness of the front legs. There are several indications that the
climate at the close of the Cretaceous was becoming drier and the
organization of the giant reptiles became modified accordingly. They
survived successfully for a while, but were ultimately replaced by the
mammals, perhaps as a result of still further change in the climate
(see p. 538).

18. Order *Pterosauria

The Triassic archosaurian reptiles gave rise to two independent
stocks that took to the air, the pterodactyls and the birds. Both of
these appear first in the Jurassic as animals already well equipped for
flight, although obviously basically of archosaurian structure. We
cannot therefore say anything about the steps by which their flight
was evolved and can only speculate about the influences that drove
them to take to the air. The early archosaurs were bipedal animals,
and the fore-limbs were therefore free and available for use as wings.
There has been much speculation about the intermediate stages by
which flight was produced. Other reptiles, such as Draco, the flying
lizard (p. 407), develop a membrane between the limbs and the body
to assist them in making soaring jumps. The flight of pterodactyls
and birds may have originated thus or, as suggested by Nopcsa, by
the flapping of the fore-limbs during rapid running on the ground,
the animals then becoming airborne for longer and longer periods.

The stages of the evolution of flight may have been different in the
two cases, for whereas the birds are obviously bipedal animals and the
similarity to such reptiles as * Strnthiomimus and *Ornithomimus is
obvious, the pterodactyls probably could not walk on their hind legs
and may have used the wing more for soaring than for flapping flight.
In spite of great differences there are interesting parallelisms in the
structure of the fully evolved fliers of the two groups, for instance the

xv. 1 8

PTERODACTYLS

427

limb bones became light, the skull bones fused, and the jaws toothless
and beaked. This parallelism in lines known to be distinct, although
of remote common origin, is similar to that which we have noticed
before in aquatic animals, and it can be interpreted as showing that

f¥.

Fig. 248. The skeleton of a pterodactyl.

A, extra wrist bone; C, coracoid; D, elongated digit; F, femur; FF, fin; H, humerus;
MC, metacarpal; P, pelvis; RU, radio-ulna; SC. scapula; ST, sternum; 7', tail; TF.
tibio-fibula; lowing. (From Thompson, The Biology of Birds, Sidg\vick& Jackson, Ltd.)

populations with similar genotypes will respond to similar environ-
mental stimuli in the same way.

The pterodactyls are most commonly found in the Jurassic strata,
less often in the Cretaceous. Many specimens have been found in
marine deposits and seem to have been fish-eaters. The characteristic
features that have produced the pterodactyl structure from a thecodont
ancestry may be described as a lengthening of the head and neck,
shortening of the body and ultimately of the tail, lengthening of the
arms and especially of the fourth digit, shortening of the legs, and
development of the ventral parts of the limb girdles. These are the

428 REPTILES xv. 18-

changes that can be recognized in the bony parts available for study;
no doubt there were many others in the soft parts also paralleling the
evolution of birds, for instance the animals may have been warm-
blooded. However, there is no evidence that they possessed feathers;
the wing was a membrane (patagium).

*Rhamphorhynchns of the Jurassic is still recognizably of archo-
saurian structure, especially in the skull, which has two fossae and
large forward-sloping teeth (Fig. 248). The fore-limb was elongated,
but the carpus still short, with an extra 'pteroid' bone in front, pre-
sumably to support the wing. The first three digits were short and
hooked, the fourth long, supporting the wing, and the fifth absent.
The hind-limb was slender, with five hooked digits. There was a long
tail, ending in an expanded 'fin'. Both girdles had well-developed
ventral regions and there was a large 'sternum', keeled in front. The
scapula articulated directly with the vertebral column.

*Ptera?wdon, of the Cretaceous, showed further modifications. The
trunk became shortened to ten or fewer segments and the fore-limb
further lengthened, the carpus being long and the fourth digit much
longer than the other three. The hind-limb remained small and the
tail became very short. The very large and elongated head gradually
lost its teeth, presumably acquiring a horny beak. In the latest forms
the skull was drawn out backwards into an extraordinary process.
Some earlier related forms were only a few inches long, but *Pterano-
don itself, of the late Cretaceous, had a wing-span of 25 ft.

Zoologists have not yet succeeded in reconstructing the life of these
animals, and it is hard to see how they could have walked on land.
The membrane, which stretched between both legs and the body, and
perhaps also included the head, must have been easily torn. The
feathers of birds can be ruffled without breaking and the loss of a few
does no great harm: the bat's wing can be torn, but at least it is
supported by many digits, whereas that of the pterodactyl was a huge
continuous membrane supported by a single finger. Again it is difficult
to see how the animals can have perched ; if they hung, as the claws
suggest, was it with the front or with the hind legs? And how can
they have staged a take-off, which in birds is greatly helped by the
jump of the hind legs? It is possible that they always came to rest
hanging from cliffs, which they could leave by soaring. Even the flight
itself presents many difficulties. Although there is a sternum and a
strong humerus, neither suggests the presence of muscles sufficiently
strong to carry a creature as large as *Pteranodon. We cannot solve any
of these mysteries, but one clue is that the biggest pterodactyls were

xv. 19 EVOLUTION OF REPTILES 429

mostly, if not all, marine. The largest flying birds alive today are the
albatrosses, which use their great weight to gain height with the
increasing velocity of the wind a few feet above the sea (p. 460). It is
possible that the pterodactyls used a similar method of soaring. They
were presumably unable to compete with the birds, however, and died
out at the end of the Cretaceous, along with so many other reptiles.

19. Conclusions from study of evolution of the reptiles

Many of the conclusions that have been drawn from study of verte-
brate evolution in the water also apply to the forms that have come
on land. The fossil record leaves no doubt that almost all the popula-
tions have changed very markedly. Few forms of reptile alive today
are closely similar to any found in the Permian or Triassic periods.
Sphenodon has shown relatively less change than most others ; it may
be significant that it is found in an isolated island region (but see

P- 772).

The data are not sufficient to show the rate of evolutionary change.

We cannot be sure whether it has been constant or even continuous,

but particular types are found only from a limited range of strata and

there is little evidence that any terrestrial form remains unchanged for

more than a few million years, at most. Each type is successful for a

while and then the niche that it fills becomes occupied by another

type, either descended from the first or, more usually, from some

related stock. Thus the earliest large land herbivores were probably

the pareiasaurs; these were replaced by other reptilian types such as

the herbivorous mammal-like reptiles, and later the sauropods (in so

far as these were terrestrial) and various types of ornithischians ; then

perhaps by the hadrosaurs in the more watery habitats and the stego-

saurs, ankylosaurs, and ceratopsia on drier ground. Finally, all these

gave place to the earliest mammalian herbivores, which were in turn

replaced by others (p. 776).

Throughout early tetrapod evolution there is a tendency to return
to the water, perhaps under some pressure of competition from
descendants on land. This is marked among reptiles, where besides
the chelonians and ichthyosaurs and plesiosaurs there are the phyto-
saurs and crocodiles, and among Squamata the mosasaurs and tylo-
saurs, not to mention the sea-snakes.

The large size of many reptiles has been one of their most striking
features, but it is, of course, not true to say that there is a strong
tendency for size to increase in all reptile groups. While many
have become enormous, others, such as the lizards, have produced

43 o REPTILES xv. 19

probably as great a biomass spread over a large number of small in-
dividuals. Large size in a reptile may help to conserve heat (p. 372),
but could also endanger the animal from overheating, since the ratio
of surface area to volume decreases as the absolute size increases, and
heat cannot be lost so readily through the skin. Up to a point size may
be a protection, but it involves the dangers of those who place all the
eggs in one basket ; incidentally, the actual eggs of these large animals
must have provided formidable physical problems for their support.

Parallel evolution of several lines descended from a single stock is
as common among reptiles as among other groups of vertebrates.
Thus the bipedal habit, with hind legs longer than the front, has been
adopted independently by a number of diapsids; again, elongated jaws
are found among fish-eaters, whether ichthyosaurs, plesiosaurs, phyto-
saurs, crocodiles, or mosasaurs.

Although it is difficult to see in all this any persistent tendency
except to change, yet the very fact that each type is so rapidly replaced
suggests that descendants in some way more efficient are continually
appearing. In the case of the reptiles the more interesting of these
are the birds and mammals, and we shall therefore leave the problem
of serial replacement among amniotes for later discussion. Meanwhile
we may note once again that the reptiles surviving today, although not
of larger size nor obviously better suited for life than their mesozoic
ancestors, yet exist in considerable numbers alongside and even in
competition with the birds and the mammals.

XVI

LIFE IN THE AIR: THE BIRDS

1 . Features of bird life

The quality we define as 'life' is perhaps more fully represented in
birds than in other vertebrates, or indeed in any animals whatsoever.
It is difficult to find units by which accurate comparisons can be made
of such matters, but there is a meaning in the statement that the life of
a bird is more intense than that of, say, a reptile or a fish. Following
out our definition of the life of a species as the total of the activities by
which that particular type of organization is preserved, we shall find
that the birds have many and very varied activities, by means of which
a great deal of matter is collected into the bird type of organization.
Moreover, this is achieved under conditions remote from those in
which life first arose; the birds get a living by moving in the air, the
most difficult medium of all.

Flight is of course the characteristic that gives us most fully the
feeling that the birds are active animals ; it impresses us as a technical
marvel and as a means by which the animals obtain a most enviable
and valuable freedom, enabling them to avoid their enemies and to
seek new habitats. Almost equally important items in the active life of
birds are the high and constant temperature and large brain. These
features have been acquired independently by birds and mammals,
and have led to profound changes in behaviour. A homoiothermic
animal does not need to change its activity with the changes in environ-
mental temperature; it can be continuously active, and, perhaps even
more important, its steady continuity of life makes possible the accurate
recording of past experience in the memory. Probably only with a high
and constant temperature can full use be made of the possibilities of
delicate balance of activities within large masses of nervous tissue. In
homoiothermic birds and mammals we find larger brains and more
elaborate social and family habits than in any other animals.

2. Bird numbers and variety

Flight necessitates a large surface-weight ratio, therefore birds do
not become so large as some mammals; nevertheless, an immense
biomass is produced by their very large numbers. Any attempt to
enumerate the bird population is largely guess-work, but the density
of breeding birds in different habitats in Britain has been estimated,

432 THE BIRDS xvi. z-

and varies from 200 per 10 acres in woodland to 20 on agricultural land
and 10 or less on moorland. Calculating from such figures Fisher
estimates that there may be 100 million land birds in Great Britain
and 100,000 million birds in the world altogether, including sea birds.
This is perhaps a low estimate ; it would represent a total biomass of
the same order as that of 3,000 million human beings. With all their
activity, therefore, the birds organize less matter into themselves than
do the mammals.

One of the most striking features of bird life is that although the
basic organization remains fairly constant differing types show a great
variety of special features, fitting them for numerous habitats. Besides
differences in behaviour, in body form, and in powers of flight there
are found others in the shape of the bill, and hence of food habits, and
in the details of many other parts, such as the feet, that make fascinat-
ing studies in adaptation to environment.

3. The skin and feathers

The skin of birds differs from that of mammals in being thin, loose,
and dry; there are no sweat glands, indeed the only cutaneous gland
present is the uropygial gland or preen gland at the base of the tail.
The bird cleans its feathers with its beak, obtaining oil from this gland,
which is especially well developed in aquatic birds.

The keratin-producing powers of the skin are of course mostly
devoted to producing feathers, but scales like those of reptiles are
present on the legs and feet and sometimes elsewhere. The bill (p. 466)
and claws are also specialized scale-like structures and are sometimes
moulted.

Nerve-endings are present throughout the skin, and the cere at the
base of the bill is perhaps an organ of touch. The bill may itself have
special endings, such as the corpuscles of Grandry found in the ducks.

The feathers of modern birds provide a covering whose uses vary
from heat insulation and flight to protective coloration and sexual
display. It is likely that in evolutionary history the function of heat
regulation came first. The two main functions of heat conservation and
flight are indeed today performed by feathers of different types (Fig.
249). The down-feathers or plumules, which form the covering of the
nestling and may be present also in the adult, are simpler than the
contour feathers or pennae, and the elaborate flattened flight feathers.
Filoplumes are a third type, being very fine, hair-like feathers. Usually
several generations of feathers are produced ; first the nestling feathers
(neoptiles), then one or more generations of juvenile feathers, which

xvi. 3

FEATHERS

433

Fig. 249. Various types of feather.

A, filoplumes; B, nestling down-feather; C, primary wing feather of pigeon; D, permanent

down feather; E, feather with free barbs; F, emu's feather with long aftershaft; G, contour

feather of pheasant with aftershaft. (Partly after Thompson, The Biology of Birds,

Sidgwick & Jackson, Ltd.)

may be of various types, prefiloplumes, preplumules, and prepennae;
finally, the adult feathers (teleoptiles).

Each feather, of whatever type, is formed from a dermal papilla or
follicle, over whose surface keratin is produced. In down-feathers the

434 THE BIRDS xvi. 3

surface of the papilla is ridged all round and the result is to produce a
number of fine threads or barbs of keratin, covering the body with
a coat of fluff, which acts as a heat insulator by preventing air circula-
tion.

Feathers, like other epidermal structures, are moulted, either at a
certain stage in the life-cycle or seasonally, a new generation being

d flflb

v. r /

Fig. 250. The structure of a feather.
I. Whole feather showing calamus (quill), C; rhachis (shaft), R; and vane, V. On the right
side a small area is shown as it appears under a lens; B, barb; Bs, barbule. II. A section cut
at right angles to two barbs in the plane of the barbules of the anterior series (Bsa). Note
how the hamuli, H, of the anterior barbs interlock with ridges (r) on the posterior barbules
{Bsp). III. Shows one anterior and two posterior barbules isolated. (After Pycraft, A History
of Birds, Methuen & Co., Ltd.)

produced from the old papillae. Most birds moult after the breeding-
season, some a second time during the year. The down-feathers of the
nestling are partly replaced by contour feathers; the follicle, instead
of producing equal barbs, now forms two large ones at one side, which
together become the central axis (rhachis), carrying a series of further
barbs that spread at right angles to it to form the vane (vexillum). Each
feather (Fig. 250) thus consists of a central rhachis, forming the hollow
calamus or quill below and carrying the barbs, which make the vane.
The calamus opens at the base by the inferior umbilicus, the entrance
of the mesodermal papilla, and at the beginning of the vane there is a
second hole, the superior umbilicus. At this point there is often a loose

xvi. 3 FEATHERS 435

tuft of barbs or an extra shaft, the aftershaft, perhaps in some way
representing the down-feather.

The barbs or rami that make up the vane are held together by rows
of barbules (radii) running nearly at right angles to the barbs and
carrying hooks (hamuli) by which the barbules of one radius become
fixed to grooves in those of the next (Fig. 250). Anyone who has played
with a feather knows that these connexions can be broken down so that
the barbs become separate, but can be joined again by 'preening' the
whole feather.

The feathers are provided with muscles at the base and the control
of their position is important for the regulation of heat loss, for flight,
and in many other activities, for instance sexual display. Like the hairs
of mammals the feathers are also used as organs for the sensation of
touch, nerve-fibres being wound round the base of the papilla. In owls
and other night-birds special vibrissae, analogous to those of mam-
mals, are present. Various specialized feathers are used for eyelashes,
ornament, and other purposes, and in some birds patches of special
feathers without rhachis break up to make a greasy 'powder down'.

The feathers are not spread uniformly over the body but are localized
to certain tracts, the pterylae, separated by bare areas, apteria. Among
the contour feathers it is usual to recognize the remiges of the wing
and rectrices of the 'tail'. The former are divided into primaries on
the hand and secondaries on the forearm (Fig. 256). Each large feather,
whether in wing or tail, is usually covered above and below by several
rows of upper and under coverts. In many birds there is a peculiar gap
in the secondary feathers of the wing, the fifth remex feather being
absent (diastataxis); the condition in which this feather is present is
called eutaxis. The feathers have a remarkably flexible structure, so
that they adopt different shapes with different positions of the wing.
The shape of the quill and barbs varies between feathers and parts of
a feather, for instance the barbs at the tip of the primary feathers
provide a stream-lined cross-section, like that of certain aeroplane
propellers (p. 453). The small covert feathers at the front of the wing
stand up vertically, but have a right-angle bend, thus providing the
wing camber.

The rectrices vary greatly, being almost absent in birds that live
near to the ground, such as the wrens, but very large in fast-moving
birds that change direction quickly (swallows). In these latter the outer
rectrices are enlarged for steering purposes. The rectrices may be put
to special uses, as in the woodpeckers, where they make a rigid brace,
or in the peacocks, whose display feathers are the tail coverts.

436

THE BIRDS

xvi. 4-

4. Colours of birds

Birds possess colour patterns more vivid than those of any other
vertebrates, using them not only for concealment but also as the chief
means of recognition and sexual stimulation and hence as the basis of
their social life. Like other animals that live far from the ground and
move fast (primates) the birds have a poor sense of smell, often none

at all, but they have very good
vision, and in many species the
turning of discriminating eyes
by one sex upon the other has
led to the development of a very
gorgeous covering. The feathers
alter the appearance of the bird
so completely that it is not fan-
tastic to compare their effect with
that of clothing in man.

As in other animal groups the
colours are produced partly by
pigments and partly by reflection
and diffraction effects (structural
coloration). The most common
pigments are melanins, ranging
from black through brown to
yellow, and laid down in the
feathers by special cells in the
papilla. The processes of these
amoeboid chromatophores con-
vey pigment to the epidermal cells
(Fig. 251). Carotenoid pigments
(soluble in organic solvents) are also found, such as the yellow xantho-
phyll of the duck's bill and feet and the red astaxanthin of pheasant
wattles. White is usually given by reflection. In blue colours incident
light is reflected from a turbid porous layer overlying a deposit of
melanin pigment. In iridescent feathers interference of light in thin
surface films gives colours like those of soap bubbles. The more
specialized iridescent feathers produce Newton's rings, with colours
of the second and even third orders. The turacos or plantain-eaters of
Africa contain two very peculiar pigments, a copper-containing red
porphyrin turacin, which is soluble in weakly alkaline water and dis-
solves out in the rain, and the green, iron-containing turacoverdin.

Fig. 251. Deposition of pigment in feather
germ. Transverse section through a develop-
ing arm feather.

c.b. cell body of pigment cell; p. process of pig-
ment cell; r. cells forming a radius; sh. sheath of
feather germ. (After Strong, from Streseman.)

xvi. 5 COLOURS OF BIRDS 437

The actual colour patterns vary with the habits of the bird. Con-
cealing (cryptic) coloration is very common; even the brighter colours
may serve this purpose, by breaking up the outline of the bird when at
rest or in motion. Most birds are dark above and white below. The
feathers often show mottled or speckled patterns rather than a homo-
geneous colour. Finches and other birds living in the sunlit upper
branches show bright yellow, yellow-green, and blue colours, either
singly or combined. Birds living in thickets, such as the thrush and
blackbird, are usually duller brown or black. An example of disruptive
coloration that is easy to observe is the white patch on the throat of a
thrush. If the nest is approached while the bird is sitting the head is
held rigidly still with the beak upwards ; the white mark on the neck
breaks the outline and instead of an obvious bird's head there appear
only the meaningless shapes of the sides of the jaws. In most species
coloration is a compromise between concealment and conspicuous-
ness. Sometimes selection has acted so that the female is cryptic, the
male conspicuous (e.g. ducks). In hole-nesting shelducks both sexes
are conspicuous. In other birds bright colours are concealed most of
the time (e.g. the robin's red breast is underneath, many waders have
conspicuous colours under their wings).

Some colour patterns seem to make the bird conspicuous and may
be a warning of a distasteful quality. The black and white pattern
shown by the magpie may be an example of such sematic coloration;
certainly this bird is seldom preyed upon, no doubt partly because of
its large size. The conspicuous black of rooks and starlings may be
connected with their social life, making it desirable that the birds
should easily follow each other, the group being protected by the com-
bined receptors of its many members and the quick response of all
to escape movements by any one.

The protective functions of the colour often give place in one or
both sexes to garments used for communication between individuals,
for such purposes as pair formation, aggression between males, nest
site selection, or rearing the young.

5. The skeleton of the bird. Sacral and sternal girders

The arrangement of the whole locomotor apparatus is based on the
plan of the bipedal archosaurian reptiles, modified and simplified for
the purposes of flight and balancing and walking on two legs. The
bones are very light and often of tubular form, but sometimes with
internal strutting well suited to the stresses they must bear (Fig. 252).
Many of the bones contain extensions of the air-sacs; even the wing

438 THE BIRDS xvi. 5

and leg bones are pneumatized in this way in very good fliers, such as
some birds of prey and the albatross. Fusion of bones has proceeded
so far that the skeleton consists of a few hollow girders and large
plates of special shape (p. 441). This result is achieved by limiting
the joints at which movement occurs and simplifying the muscular
system. The long bones ossify from a single diaphysis, there are no
epiphyses at the ends.

The skeleton of the backbone and limb girdles is so modified as to
allow the weight of the body to be carried in two quite distinct ways,

Fig. 252. Metacarpal bone from the wing of a vulture, sectioned to show the
arrangement of the struts similar to that known to the engineer as a Warren's truss,
such as is often used in aeroplane wings. (After Prochnow and D'Arcy Thompson.)

on the wings or on the legs. For this purpose there are two plate-like
girders, the sternum and the synsacrum, curved in opposite directions.
The muscles around the shoulder and hip joints balance the weight
on these girders and produce propulsion. The main thrusts come from
the pectoralis major in flying and from the leg retractors in walking.
Perhaps no other animals are suited so perfectly for locomotion by two
distinct means, and of course many birds can swim as well as fly and
walk.

The whole axis of a bird is morphologically shorter than that of any
other vertebrate except a frog or a tortoise (Fig. 253): only the neck
remains a long and mobile structure. The number of cervical verte-
brae varies and is greater in the birds with longer necks; there are
fourteen in the pigeon, if we include two that bear ribs not articulating
with the sternum. The cervical centra have saddle-shaped surfaces,
the concavity running from side to side on the front and up and down
behind, allowing great mobility in all directions.

There are four or five thoracic vertebrae, all except the last united
into a single mass. The ribs are large, double-headed, and jointed to
the vertebrae. They bear uncinate processes on their vertebral por-
tions, hook-like projections overlapping the rib next behind and thus
strengthening the whole thoracic cage. There is a well-marked joint

xvi. s SKELETON 439

between the vertebral and sternal portions of the ribs. The latter are
bony, not cartilaginous as in mammals, and are jointed to the sternum,
which is a very large keeled structure in all flying birds, serving to

Sunsacrum
(1 thoracic, 5 lumbar
Z sacral, S caudal )

vac.

Fig. 253. Skeleton of the pigeon (Columba).

at. atlas; fl.v. axis; C12, 12th cervical vertebra; car. keel of sternum; carp, carpus; cor. cora-
coid; c.r. cervical rib; delt.r. deltoid ridge of humerus ; fern, femur ;fib. fibula ;fur. furcula;
hyp. hypapophysis; il. ilium; isch. ischium; m. auditory meatus; mc. 2 and 3, metacarpals;
pub. pubis; pyg. pygostyle; rad. radius; sc. scapula; St. body of sternum; tar. met. tarso-
metatarsus; tib.tar. tibio-tarsus; uln. ulna; up. uncinate process; vac. vacuity in side of skull.

carry the weight of the body to the wings by the attachment of the
main wing muscles (Fig. 254). The pectoralis major, which depresses
the wing in flight, is attached to the edge of the sternum and the great
depth of the keel serves to increase the length and mechanical advan-
tage of the fibres of the muscle and also, by its shape, to strengthen
the sternum. When the bird is in the air the sternum is carrying a large
part of the weight. By this arrangement the centre of gravity is kept
well below the centre of pressure, giving great stability.

44° THE BIRDS xvi. 5-

The last thoracic (rib-bearing) veitebra is united with about five
that can be regarded as lumbars, two sacrals and five caudals to make
a synsacrum, which is also fused with the ilium. This produces a very
thin plate-like structure, whose ridged shape gives it sufficient strength
to carry the bird's weight. Finally, there is a short bony tail of about
six free caudal vertebrae, carrying four that are fused together to form
the upturned pygostyle, supporting the tail feathers.

The joints of the vertebral column are therefore reduced so as to
allow movement only in the cervical region, between the thorax and

>c±ggs;

Fig. 254. Diagrams of the pectoral and pelvic girdles of an eagle, to show the methods of

support in flying and walking. In each case the weight is carried on an arch, the strength

of which is obtained by the peculiar kinked shape of the thin sheets of bone.

synsacrum and in the tail. The axial muscles have been correspond-
ingly reduced. Those of the neck are large and the hinder cervical and
the thoracic vertebrae have special ventral hypapophyses for attach-
ment of the flexor muscles of the neck. The other back muscles, except
those of the tail, are reduced and the whole back forms a single rigid
strut, carrying the weight of the breast and viscera through the ribs
and the abdominal muscles either to the pelvic girdle or to the sternum.
In flying this weight is suspended on the wings and there is therefore
a compression stress throughout the ribs, and this no doubt accounts
for the ossification of their ventral parts. The weight of the bird when
resting on its wings (Fig. 254) is thus carried by the pectoralis major
as a tension member, through the plate-like sternum; the ribs, and
especially the coracoid, act as compression members. The last-named
bone lies nearly in the plane of the pectoralis major and is very strongly
built.

6. The sacral girder and legs

In standing, perching, and walking the weight is balanced on two
legs. To achieve this posture the type of girder found in the vertebral

xvi. 6 SACRAL GIRDER 441

column of other terrestrial vertebrates has been abandoned, and with
it the system of braces (back muscles) holding up the weight of the
forepart of the body. Instead the whole axis is so shortened that the
centre of gravity lies far back, low, and over the feet. This is not

Fig. 255. Diagram of muscles of the hind leg of a bird. Tendons shown dotted.

1, Mm. ilio-trochanterici; 2, M. ilio-femoralis; 3, M. obturator; 4, M. ischio-femoralis;
5, M. caud-ilio-femoralis; 6, M. pub-ischio-femoralis; 7, M. ilio-tibialis posterior; "ja,
M. ilio-tibialis anterior; 8, M. sartorius (ilio-tibialis internus); 9, M. femoro-tibialis medius ;
ga, M. femoro-tibialis externus; 11, M. ilio-fibularis; 12, M. ischio-flexorius; 13, M.
caud-ilio-flexorius; 14, M. gastrocnemius; 15, M. peroneus superficialis; 16, M. peroneus
profundus; 17, M. tibialis anterior; 18, Mm. rlexores digitorum; 19, Mm. extensores
digitorum. si. sling for M. ilio-fibularis. (After Stolpe.)

apparent from Fig. 255, which is not in a normal perched position.
Birds whose feet are placed far back for swimming must hold the body
nearly upright to achieve a stable position with the centre of gravity
over the feet (auks, penguins). The ribs and abdominal muscles trans-
fer the weight to the greatly elongated ilia, which are fused to the
vertebrae, making a long girder of approximately parabolic form.
Though this is composed of bone of almost paper thinness, it is
strengthened by longitudinal ridges (Fig. 254). Its strength, like that
of the sternum, lies not in its arched shape in the transverse plane, but
in the distribution of weight that is achieved by its longitudinal curve
and peculiar kinked shape. The whole pelvic girdle is modified to allow

(442)

Fig. 256. Dissection of pigeon from back.

c-h. coraco-humeral; caud-il-fem. caud-ilio-femoralis; delt. deltoid; e.c.r. extensor carpi
radialis; ex.dig. extensor digitorum; ex. poll, extensor pollicis; fl.dig. flexor digitorum;
fl.met.uln. flexor metacarpi ulnaris; fl. poll. long, flexor pollicis longus; gastr. gastrocnemius;
il-caud. ilio-caudalis; il-fib. ilio-fibularis (cut); il-tr. ilio-trochantericus; int. interosseus;
isc.f. ischio-femoralis; lat.d. latissimus dorsi; lat.lig. lateral ligament of knee; m. external
auditory meatus; n. sciatic nerve; nos. nostril; per. peroneus; pub. isc. fern, pub-ischio-femo-
ralis; rh. rhomboid; sart. sartorius; sc. scapula; s.c.h. scapulo-humeral (cut); serr. serratus
anterior; 5/. sling for tendon of ilio-fibularis; t. tongue; tend, tendon of pectoralis minor;
tens. ace. tensor accessorius; tens. long, tensor longus; tri. triceps; ur.gl. uropygial gland;

vin. vinculum elasticum.

xvi. 6 LEGS 443

this arrangement. The ischium and pubis are directed backwards and
do not meet in a symphysis, which would prevent the underslinging
of the viscera.

The legs are used for balance and walking or hopping in ways that
show interesting similarities and differences from those of man. The
femur is turned under the body and articulates with the acetabulum
in such a way that movement is almost restricted to the antero-
posterior direction. The bird balances on its hips only in the sagittal
plane; there are no movements of abduction and adduction such as are
found in man. Abduction of the leg, or the falling medially of the
bird's body when standing on one leg, is prevented by the fact that
besides the ball and socket articulation of the femoral head there is
also a second joint surface between the trochanter and an anti-
trochanter of the ilium. The ligaments across the top of this joint are
very strong and they limit abduction movements, while movements
of adduction are restricted by a strong ligamentum teres attached to
the femoral head.

In life the femur is held nearly horizontal, bringing the legs well
forward. The bird replaces the movements of abduction and adduc-
tion, which we make at the hip during walking in order to prevent
falling over while only one leg is on the ground, by movements of
rotation at the knee. The muscles around the hip joint form a system
of braces allowing balancing and locomotion much as in man, but they
are well developed only anteriorly and posteriorly; the lateral and
medial (abductor and adductor) elements are weak (Figs. 255-8). The
anterior group (protractors) includes a sartorius (ilio-tibialis internus)
running from the ilium to the tibia, an ilio-femoral, and a large
anterior ilio-tibial inserted through a patella to a ridge on the front of
the tibia. Associated with this muscle, w*hich crosses both hip and
knee joints, there are also, as in man, femoro-tibial muscles, making
up with the longer muscles, the extensor system of the knee.

The lateral side of the hip joint is supported by rather small ab-
ductor braces, the ilio-trochanteric muscles, corresponding to our
glutei, and acting mainly as medial rotators, opposed by obturator and
ischio-femoral muscles, which work as lateral rotators. The main loco-
motor muscles are the posterior braces or retractors, lying behind the
hip joint and including muscles know r n as the posterior ilio-tibial,
ilio-fibular, caud-ilio-flexorius, pub-ischio-femoral, ischio-femoral,
and caud-ischio-femoral. Some of these also act with the obturator
muscle as lateral rotators, and those placed more medially function
as adductors or medial braces, so far as such are required.

444 THE BIRDS xvi. 6

The femur articulates with both tibia and fibula at the knee. The
fibula is distinct at its upper end, fused with the tibia below. The
joints of the foot are greatly simplified by the union of the proximal

Fig. 257. Leg of pigeon dissected from lateral side.
amb. ambiens tendon; dist.fi. flexors of distal phalanges ; fib. fibula; gastr. gastrocnemius;
il-fib. ilio-fibularis; il-tib. ilio-tibialis; isch-fl. ischio-flexorius; lig. lateral ligament of
knee; peron.brev. peroneus brevis; peron.long. peroneus longus; pr.fi. flexors of proximal
phalanges; sort, sartorius; sen. sciatic nerve; si. sling for tendon of ilio-fibularis; t.t. tibio-
tarsus; t.mt. tarso-metatarsus.

tarsals with the tibia to make a tibio-tarsus, articulating at an inter-
tarsal joint with the remaining three tarsal and metatarsal bones, fused
to make a single tarso-metatarsus. There are usually four digits arti-
culating with the tarso-metatarsus; three directed forwards and one
backwards. In standing, the weight is usually balanced in tripod
fashion on three of the four points provided by the front and back
portions of the feet.

(445)

Fig. 258. Pigeon dissected from ventral surface.

amb. ambiens; bas. bastard wing; br-rad. brachio-radialis; b. biceps; b.t. biceps tendon;
caud-il-flex. caud-ilio-flexorius; cl. clavicle; c.br. coraco-brachialis; cor. coracoid; d.II.
2nd digit; e.c.r. extensor carpi radialis; ex. extensor; ext.obl. external oblique; fl.carp.uln.
flexor carpi ulnaris; gastr. gastrocnemius; oes. oesophagus; il-tib. ilio-tibialis; int. obi.
internal oblique; lig. lateral ligament of knee; nic. nictitating membrane; pect. pectoralis
major; p.m. pectoralis minor (supracoracoideus); per. long, peroneus longus; pr.long. pro-
nator longus; pub-isc-fem. pub-ischio-femoralis; sart. sartorius; tens.acc. tensor accessorius;
tib.ant. tibialis anterior; trac. trachea; tri. triceps; uln. ulnar.

446 THE BIRDS xvi. 6-

The knee joint has some remarkable similarities to that of man. It is
stabilized by lateral, medial, and cruciate ligaments and contains a pair
of lunate cartilages or 'menisci'. The joint allows movements of flexion
and extension and the femur as it extends on the tibia in walking
rotates laterally because of the arrangement of the joint surfaces. The
bird thus balances in the medio-lateral plane by rotation at the knee,
somewhat as we do by abduction-adduction at the hip (Fig. 259).
When it makes a step forward the weight is brought by this rotation
at the knee over the leg that remains on the ground.

Fig. 259. Drawings from photographs of a goose, A, standing; B, step-
ping. The centre of gravity S is brought over the foot on the ground by
lateral rotation of the femur on the tibia. Note the position of the tail
in B. (After Heinroth, from Stolpe.)

The intertarsal joint allows mainly movements of flexion and exten-
sion. It is largely supported by ligaments and has a very strong capsule
and lateral and cruciate ligaments rather like those of the knee; there
is even a meniscus on the lateral side. The back of the tibia is occupied
by the gastrocnemius and the flexor muscles of the toes and at the front
there is a tibialis anterior acting across the inter-tarsal joint, and also
extensors of the toes. The calf muscles are mainly concerned with pro-
ducing flexion of the toes in the act of perching and they form an
elaborate system of tendons attached to the phalanges. These tendons
often act as a single unit, and there is an arrangement by which the
flexion is passively maintained by the weight of the body, even during
sleep. Many of the muscles are specially arranged to allow support of
the joint whether in the flexed or extended position. The ilioflbular
muscle passes through a conspicuous sling for this purpose (Figs. 255
and 257). The flexor muscles of the toes are inserted largely above the
knee and thus tend to tighten as the bird sinks. In this they may be
assisted by the ambiens, a muscle found in reptiles and some birds,
which takes origin from the ilium. The muscle belly lies on the medial

xvi. 7 SKELETON OF WINGS 447

side of the thigh, and its tendon runs beneath the patella on to the
lateral surface of the lower leg, where it is attached to the upper end
of the muscles that flex the toes. This arrangement provides a single
string crossing hip, knee, and ankle and allows the weight of the body
to flex the toes as the joints bend.

The second mechanism for maintaining the bird on its perch is a
locking device that holds the toes flexed. The under-surface of the
flexor tendon is ridged at the metatarso-phalangeal joint, where the
weight of the body presses it against a branch. The upper side of
the tendon sheath is also ribbed and as the bird settles on its perch
the two sets of ridges interlock.

The feet show a wide variety of adaptations for special habitats (Fig.
260). In the cursorial and walking birds there are often long digits in
front and behind to give a long base for balance, but the number may
be reduced — to two in running birds, such as the ostrich. Hopping is
used by small birds on the ground and in the trees and produces quick
movement. It is expensive because of the large displacements of the
centre of gravity, and for long distances or large animals walking is
more efficient. Many different groups of birds have acquired webbed
feet for swimming. In birds exposed to cold the digits may be enclosed
in a coat of feathers. Birds of prey develop long raptorial talons.
Throughout the great group of perching birds one digit is directed
backwards, allowing firm grasp of a branch. In climbing birds the
fourth digit is often directed backwards as well as the first, so that the
foot forms a sort of pincer, with long curved claws.

7. Skeleton of the wings

The wing is designed to have a minimum moment of inertia about
an axis parallel to the sagittal plane and passing through the shoulder
joint. Movements are produced by muscles lying either outside the
arm or in its proximal part, with long tendons. The wing feathers are
carried along the post-axial border of the humerus, ulna, and hand,
and the shape of the wing depends on the position in which the feathers
are held by their muscles, as well as on membranes, the pre- and post-
patagia, developed where the limb joins the body. The active move-
ments of flight are produced mainly by the pectoral muscles; the joints
and muscles of the wing itself serve to spread the wing and to adjust its
shape during each beat. The humerus is short and broad with a large
head and an expanded surface for attachment of the pectoral muscles.
Radius and ulna are both large, especially the latter. There are only
two free proximal carpals and the remainder of the wrist is formed of

448

THE BIRDS

xvi. 7-

three metacarpals, one short and two long and fused. Only one digit,
probably representing the second, is well developed, having two broad
phalanges; the third and the first digits consist of single rods, the

Fig. 260. Various types of feet in birds.

1, shag (swimming); 2, crow (perching, lifting); 3, ptarmigan (stockinged by

feathers); 4, jungle fowl (walking, scraping); 5, coot (lobate, swimming); 6, jacana

(suited for walking on floating plants); 7, sea-eagle (raptorial). (From Thompson,

Biology of Birds, Sidgwick & Jackson, Ltd.)

latter, standing somewhat apart at the front of the base of the hand, is
capable of independent movement ; it carries the bastard wing (alula or
ala spuria).

The glenoid cavity is formed at the union of a blade-like scapula and
a stout coracoid. The former lies horizontally and is attached by
muscles to the vertebral column and ribs. The coracoid holds the wing

xvi. 8 WING MUSCLES 449

away from the sternum, with which it makes a joint. The furcula,
probably consisting of the combined clavicles and interclavicles, is
loosely attached to the sternum and carries the origin of muscles that
rotate the humerus about its long axis.

8. Wing muscles

Depression of the wing is produced mainly by a single mass of
muscle, the huge pectoralis major, making up as much as one-fifth of
the whole weight of the body. It runs from the sternum and furcula to
the under side of the humerus, to which it is attached, at some distance
from the joint, by a complicated tendon of insertion. The fibres of this
muscle are very red in strongly flying birds and often contain numerous
lipoid inclusions. In the fowl the fibres are white and contain glycogen,
but little lipoid. Elevation of the wing is produced by a muscle also
attached to the sternum, lying deep to the pectoralis major and often
called the pectoralis minor, but more properly supracoracoideus. Its
tendon passes through the foramen triosseum, between the furcula,
scapula, and coracoid, to be inserted on the upper side of the humerus.
It is assisted by latissimus dorsi and deltoid muscles.

The chief muscles of the shoulder are thus a massive set serving to
raise and lower the wing. There is little development of the other
muscles such as are present in other vertebrates for the purpose of
balance and drawing the limb backwards and forwards for standing
and locomotion. Such a system of braces all round the joint is unneces-
sary; the bird balances on its wings mainly by the action of the pec-
toralis major as the chief brace, between the sternum and the humerus,
with the coracoid as a compression member between. Stresses must of
course arise in other directions besides those tending to produce a
vertical fall and these are met by the muscles that produce rotation of
the humerus and various other movements of the wing, especially a
pronation, depressing the leading edge. The muscles used in other
tetrapods to sling the weight of the body to the pectoral girdle and
fore-limb are little developed. The scapula is held to the vertebral
column by small rhomboid muscles and there is a short series of slips
attached to the ribs, the serratus anterior.

Other muscles running from the body to the humerus produce
rotation of the humerus at the glenoid and adjustments of the patagia,
movements that are very important in flight. From the outer surface
of the scapula arises a scapulo-humeral muscle, inserted in such a way
as to produce adduction and lateral rotation of the humerus, raising
the hinder edge of the wing. The coraco-humeral muscle is a compact

bundle attached near to the last and producing the opposite effect of
abduction and medial rotation, lowering the hinder aspect of the wing.

The deltoid muscle is divided into several parts and besides its main
abductor action on the wing also has slips inserted into the skin of the
anterior patagium, muscles known as the long and short tensors of
that membrane. There is also a tensor accessorius, running from the
surface of the biceps to the skin of the leading edge of the wing.

The muscles within the arm itself serve to extend or fold the whole
wing and to alter the positions of the parts, especially by pronation and
supination during flight. Large triceps and smaller biceps muscles act
at the elbow. In the forearm there is a large extensor carpi radialis and
an extensor carpi ulnaris, serving to keep the wing extended at the
wrist. Flexor carpi ulnaris folds the wing. There are also two large
pronators, brevis and longus (brachio-cradialis), rotating the radius
medially and lifting the back of the wing. A system of digital flexors
and extensors, inserted into the distal phalanx of the main digit, keeps
the wing tip spread out or folds it. The position of individual feathers
is controlled by an elaborate system of tendons and muscles along the
back of the hand. The first digit is moved independently by abductor
and adductor pollicis muscles, controlling the position of the bastard
wing, which increases the angle of stall and thus allows slow flying
speeds in take-off and landing.

9. Principles of bird flight

A plane surface moved through the air in a direction inclined at an
angle to this plane is known as an aerofoil. The forces generated can
be resolved into a lift force acting upwards and a drag force tending to
stop the motion. On this fact depends the power of supporting weight
in the air that is possessed by birds and human heavier-than-air
machines. Both lift and drag forces are proportional to the square of
the speed, and the requirement for sustained flight in still air is that
the object shall have sufficient speed to generate a lift force equal
to its weight.

The flow of air over the upper surface of the wing reduces the
pressure there and provides the main portion of the lift (Figs. 261-2).
By tilting the wing (increasing the 'angle of attack') the pressure on the
underside can be increased, but the air flow now tends not to follow
the upper surface but to become turbulent, especially at the hind edge,
destroying the lift (Figs. 261-2). When an aerofoil falls below this
critical speed it stalls; that is to say, drops suddenly, being no longer
supported. The smooth flow of air over the wing tends to be especially

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452 THE BIRDS xvi. 9-

disturbed at its hinder ('trailing') edge and by eddies round the end
('tip vortex'). The proportion of length to breadth (aspect ratio) in the
wing suitable for a particular type of flight depends on the need to
provide a sufficiently large undisturbed area.

The shape of the aerofoil is of critical importance in determining its
aerodynamic capacities. For birds, as for aeroplanes, there are differing
shapes, suitable for various types of flight. To understand them we
must classify the means by which birds attain the necessary forward
velocity. First and most obvious is flapping flight. Though the details
of this are varied and not fully understood, it can be regarded as a
screw-like motion of the wings, providing forward and upward com-
ponents (p. 455).

In still air the only alternative to flapping flight is to glide down-
wards, which obviously cannot continue indefinitely. Yet some birds,
such as the gulls, and especially the albatrosses and the buzzards,
condors, and other birds of prey, can be seen to soar for many minutes,
gaining height without flapping the wings. Lord Rayleigh showed how
they can do this by making use of the fact that the air is seldom still.
Theoretically the bird can use three types of air movement : (1) ascend-
ing currents, usually thermal ; (2) variations in the wind velocity at any
one level (gusts); (3) differences in wind velocity at different levels.
The first method is that used by human sail-planes and is certainly
adopted by many soaring land birds. The gustiness of the wind is
probably turned to advantage by gulls, rooks, and many other birds,
and the decrease in wind velocity near the sea surface is used by marine
soaring birds, notably the albatross.

10. Wing shape

A wing of the shape that allows an albatross or swift to make its
superb manoeuvres would stall immediately at the speed of flight
adopted by a crow. In discussing wing shape the chief factors to be
considered are (1) the wing area, (2) the aspect ratio (wing length/
breadth), (3) the w 7 ing outline and taper, (4) the presence of holes or
slots, (5) the camber or curvature of the wing.

1 1 . Wing area and loading

A small wing area is necessary for fast flight, since the dragoc areaX
speed 2 , at least for high speeds. For this reason fast aeroplanes and
birds have small wings, but in the bird the fact that the wing provides
the forward momentum as well as the lift greatly complicates matters.
For flapping flight the wings must be moved relatively fast and for this

xvi. i 3 ASPECT RATIO 453

small size is an advantage. On the other hand, a large wing area allows
slow flight (lift oc area X speed 2 ) and is found in hawks, vultures,
storks, and other birds that fly slowly to hunt, especially if they soar
on thermal currents, for which a large lift is necessary (p. 458).

The loading of the wing varies considerably. Since the weight
increases with the cube but the wing area only with the square of the
linear dimensions, it follows that large birds must have relatively larger
wings than small. However, the larger birds usually have a heavier
loading of the wing, for instance, 10 kg./m. 2 in the duck (Anas), 20 in
the swan (Cygnns) , 1 in the goldcrest (Regains), 3 in the crow (Corvus).
A considerable 'safety margin' remains in most birds; for instance,
pigeons were found to be able to fly until as much as 45 per cent of
the wing surface was removed ; hawks and owls have an especially high
safety margin and they can carry prey almost as heavy as themselves.

12. Aspect ratio

Although a small wing area reduces drag, many fast-flying birds
have a large wing-span. The aerodynamic advantages of this allow a
low rate of descent when gliding, reducing the expenditure of energy
necessary to sustain flight. High aspect ratio is therefore found in birds
that fly fast by flapping flight (swifts and swallows) and especially in
those, such as the albatross, that glide fast in order to obtain sufficient
kinetic energy to convert into altitude. However, these wings with very
high aspect ratio stall at relatively high speeds and the birds that soar
slowly on thermal up-currents over the land mostly have a low aspect
ratio. Some figures for aspect ratios are:

Albatross (Diotnedea) . . .25

Gull (Lartis) . . . .11

Swift (Apus) . . . .11

Shearwater (Puffinus) . . .10

Vulture {Neophron) . . .6

Rook (Corvus) . . . .6

Sparrow (Passer) . . . .5

13. Wing tips, slots, and camber

A pointed wing tends to stall first at its tip and is therefore only
suitable for fast fliers. Such birds show great development of the hand
feathers, producing a long narrow wing, whereas birds built for slower
flight and manoeuvre have a shorter broader wing with long arm
feathers (Fig. 263).

The condition of the air around the wing is of first importance for
the maintenance of lift; if there is not a smooth stream over the upper
and under surfaces the air becomes turbulent, and the aerofoil stalls
(Figs. 261-2). This tends to happen either if the speed falls too low or if
the angle of the wing relative to the line of motion increases above about

454 THE BIRDS xvi. 13-

20 . Turbulence is mitigated, however, by the provision of openings,
known as slots, which let through part of the air and provide the
necessary smooth stream. The spaces that occur between the feathers,
especially towards the wing tip, almost certainly function as slots.
Probably the arrangement provides a series of such apertures, giving
a very efficient high-lift device. Such slots are conspicuous in slow

Aca'piter

Fig. 263. Wings built for speed (falcon, Falco) and for manoeuvring
(hawk, Accipiter). The former is long and narrow, with relatively
large hand feathers. The latter is short and broad, the arm feathers
being long and the primaries arranged to make slots. (After Fuertes.)

fliers (rooks) and especially in those that soar on thermal up-currents
(vultures). The feathers of such birds are often individually tapered
(Fig. 263). Slots are also found in the wings of large birds that are fast
fliers (pheasants), the wing being liable to stall in certain phases of the
down strokes. It is possible that the bastard wing acts as a slotting
device; indeed, consideration of it played a part in development of the
theory of turbulence and slotting.

The shape of the wing has a very important influence on the air
stream. In most birds there is a stiff leading edge and a thinner trailing
edge. Nearly all wings are cambered, that is to say, they taper from
the leading to the trailing edge, especially in the region of the forearm

xvi. 14

FLAPPING FLIGHT

455

(Figs. 261-2). This arrangement directs the air stream over the upper
surface of the wing in such a way as to provide an extra lift by creating
a 'suction zone' of reduced pressure. How T ever, high camber, like low
aspect ratio, reduces the speed of the bird.

14. Flapping flight

Flapping flight involves a complex,
screw-like motion of the wing, down-
wards and forwards then upwards
and backwards, more rapid upwards
than downwards (Fig. 264). The
action of the wings differs during
take-off or landing from that in sus-
tained flight (Brown, 1953). In the
former conditions, when the speed
is slow, forward velocity is provided
by backward movement of the wings.
During each stroke, beginning with
the wings raised, they are first moved
downward and then forward, pro-
viding lift (Figs. 264, 265). This
movement is produced mainly by
the pectoralis major. During the
upstroke the wing is first adducted,
folded and flexed, and supinated at
the wrist, by the actions of pectoralis

minor and other muscles. A very rapid backward flick then follows,
produced by upward and forward rotation of the humerus, extension
of the wing, and pronation of the manus. The effect of these move-
ments, produced largely by the triceps and other extensors, is to
provide a forward component.

This form of flight involves mainly the primary feathers. It is
evidently very tiring and can only be continued for a few seconds. In
sustained flight the downstroke is as in slow flight but the upstroke is
much simpler, with only a slight backward flick of the primary feathers.
The action is such that the inner part of the wing provides lift, the
tip propulsion. The upstroke in fast flight is thus mainly passive,
produced by the pressure of air against the under surface. The major
part of the effort needed to provide lift and forward propulsion is thus
provided by the pectoralis major. This muscle weighs as much as one-
fifth of the body weight in flappers, such as the lapwing, as little as

Fig. 264. Pathway of the wing tip and
wrist joint relative to the body during
free flapping flight of a gull. Equal
time-intervals are shown. Note the
great speed of the upward beat and
that the forearm is raised before the
wing tip. (After Demoll.)

(456)

Fig. 265. Pigeon (Columba) with wings at bottom of stroke during rising. From a

photograph taken at very short exposure. Note forward position of wings but

upward and backward curled primary feathers. (After Aymar.)

■UW'.

m^.

Fig. 266. Drawings from four photographs from film of a take-off by an eagle
(Aquila). A. The legs are jumping and the upper arms nearly vertical before the
wrist joint is extended. B. Wing fully extended with bastard wing spread out,
some pronation. C. Marked pronation as the upper arm reaches its lowest point.
D. The upper arm is proceeding upwards, although the hand has not yet reached
its lowest point. (Drawn from photographs by Knight, from Streseman.)

xvi. i 4 FLAPPING FLIGHT 457

one-ninth in soarers, such as the gull. It does nearly all the work, the
other muscles serving to give extra lift when needed.

The feathers are held by an ela-
borate system of tendons and in
some birds they are allowed to
twist only when the wing is being
raised and the barbs of the
feathers themselves are so ar-
ranged that they open like the
vanes of a blind when unaer
pressure from above, but close
when the pressure is from below
(Fig. 268). In other birds, especi-
ally those that fly fast with a slow
wing beat, such as gulls and
swans, the wing is probably rigid
on the up as well as on the down

Fig. 267. Bill-fisher leaving its hole in a
bank, showing wings half-way through the
upstroke. The upper arm has reached its
highest point and the forearm is just starting
upwards; its primary feathers have opened
on the right wing, reducing resistance.
(Drawn from photograph by Aymar, Bird
Flight, published by John Lane, The Bod-
ley Head, Ltd.)

strokes, and is twisted so as to

produce forward and upward components on the up stroke

vinculum

PRIMA

RIBS

5 6 78 910 II 12 13 #.
S £CO/VDARlE S

Fig. 268. Diagram of wing to show arrangement of the flight feathers.
(From Pycraft, A History of Birds, Methuen & Co., Ltd.)

The whole upward movement is usually faster than the downward
one. Before the wing tip has reached its highest point the upper arm
is already beginning to descend and in this way the line of flight is

45«

THE BIRDS

xvi. 14-16

maintained almost straight and does not follow a wavy path as it would
do if the parts of the wing vibrated together. In small birds the wing
works more nearly as a whole and the flight differs in several respects
from that of larger birds. In general the wing is a very labile system
and regulates itself automatically with changes in the aerodynamical
forces. This regulation is produced partly by feather plasticity and
joint mobility, with participation of reflex muscular adjustments that
are little understood.

The whirring flight of some small birds, especially of humming
birds, enables them to remain almost in one
place in the air, or even to move backwards.
The wings beat backwards and forwards
(Fig. 269), often as fast as 200 times a second,
and the 'pectoralis minor' is almost as large as
the major.

15. Soaring flight

Many birds economize the energy needed
for flapping flight by making skilful use of
the possibilities presented by movement of the
air. All birds glide for short distances, some
small birds with wings folded, others with
wings outstretched. Sustained gliding and
soaring upwards without flapping the wings
is found only in large birds, probably because
considerable weight is necessary to provide
kinetic energy sufficient to ensure continuous
flight and efficient use of wind variations. As
has been suggested, there are two distinct types of soaring birds:
(1) land birds using thermal up-currents, (2) marine birds using
variations in wind above sea level.

Fig. 269. Spotted fly-
catcher hovering. The
wings are passing back-
wards and there are spaces
between the feathers.
(Drawn from a photo-
graph by E. Hosking,
with permission.)

16. Soaring on up-currents

Up-currents of air arise in the neighbourhood of large objects on
the ground (cliffs or even a ship) and particularly from variations
in the rate of heating of the earth's surface in the sun, over rocks,
vegetation, mountain shadows, &c. Birds using such currents usually
proceed upwards in a series of small circles, a behaviour seen in
buzzards and other hawks and especially characteristic of vultures,
which may ascend in this way above 1,000 ft (Figs. 270-2). The
characteristic features of such thermal soarers are large wing area,

(459)

wind

FlG. 270. Flight of an eagle (Aquila).

a-b, flapping flight; B-C, soaring at constant height; C-D,
soaring in ascending spirals; d-e, gliding. (After Ahlborn.)

Fig. 271. Soaring flight of kite (Milvus).

Losing height downwind and gaining it upwind. Time-marks one second.
(After Hankin.)

Fig. 272. Wings of vulture (Gyps).

A, soaring upwind, gaining height; B, upwind on level; c, downwind, losing height;
D-F, gliding flight. (After Ahlborn.)

460

THE BIRDS

xvi. 16-

low aspect ratio, and wings broad at the tip and usually provided
with well-marked slots.

17. Use of vertical wind variations

The decreasing effect of surface friction causes the wind to blow
faster at greater heights and this phenomenon is used by some birds
at sea, where conditions are presumably more uniform than over the

Fig. 273. Wings of the albatross (Diomeded), used for soaring flight. Wing very
narrow, with long upper arm region. (Drawn from photograph by Aymar.)

land. The albatross (Diomeded) (Fig. 273) is the classic example of this
type of bird, proceeding in a regular series of movements, without
flapping the wings, downwind losing height and gaining speed and
then upwind gaining height and passing into a faster-moving layer.
Each downwind tack is longer than the upwind one. During the upwind
tack the wings are spread forwards, downwind backwards. The alba-
tross remains all the time within 50 ft of the sea surface, because the
variations in wind velocity are marked only at low levels. The
albatross shows the characteristics suitable for this type of flight,
namely, large size (it is the largest of all flying birds), great wing span
(11 ft), high aspect ratio (25), and pointed wing tips, without slots.
Other sea birds, such as the gulls, though not so highly specialized,

xvi. 1 8

SPEED OF FLIGHT

461

can take advantage of variations in horizontal wind velocity, including
gusts at any one level. The bird moves upwards as it meets an accele-
rating gust and turns when the wind decelerates. Gulls also use up-
currents at cliff faces and, no doubt, air movements of all sorts are

Fig. 274. Heron (Ardea) leaving its perch. The legs have been used to make a jump
and the wings are fully spread. (Drawn from photograph by Aymar.)

widely used, especially by large birds. However, it is evident that the
wing equipment only allows the bird a limited range of choice and
probably even the slightly different wing shapes of related species
depend on the differing conditions they are called upon to meet. A
vulture could no more zoom backwards and forwards over the waves
than an albatross could circle slowly on a gentle thermal up-current.
A pigeon cannot equal a gull at steady gliding and soaring, but the
pigeon can rise more steeply or descend more rapidly without stalling.

18. Speed of flight

Estimation of the speed of flight involves distinguishing between air
and ground speed. The speed relative to the ground may be very high ;
there are records of birds covering more than 100 land miles in an

462

THE BIRDS

hour, with the help of the wind. Racing pigeons can average 40 miles
an hour or more for considerable periods. Air speeds of 30-50 m.p.h.
can certainly be reached by many birds: swifts are said to reach 100
m.p.h. in still air.

Fig. 275. Pigeons (Columba), photographed during take-off, with exposures of
1/825 second. A, front, and b, rear view, with wings together, c, nearly, and d,
quite at bottom of downstroke; note pronation and forward movement of wing.
E and F, wings during the upstroke; in f the primary feathers have opened; note
that the wing moves backwards and that the motion is faster than on the down-
stroke. (From photographs by Aymar.)

19. Take-off and landing

At the take-off the bird has to acquire sufficient forward momentum
to provide lift, and yet must leave the air sufficiently undisturbed for
subsequent beats to be effective. In many birds, especially the smaller,
the jump provided by the legs is adequate for the take-off (Fig. 274).
Large birds must run or swim rapidly to obtain sufficient speed. Eagles
are said to be unable to rise without a long run, and many large birds
nest on a cliff or tree, which gives them an up-current for the take-off.
Swifts usually come to rest high up and can only rise off the ground
with difficulty. The albatross is unable to take off from the sea surface
in a dead calm.

The first beats are usually very large, beginning with the wings
above the back and held at such an angle as to produce a large forward

xvi. 19

LANDING

463

component. The wings may be heard actually clapping together in
pigeons (Fig. 275). During rapid ascent, as in the larks, the body is
nearly vertical and the wing changes its angle at the shoulder very

Fig. 276. Jackdaw about to land.
The wings are fully extended on
the downbeat, and the tail is
fanned out and bent downwards.
(From photograph by Aymar.)

Fig. 277. Hawk striking at a dummy owl.
Note long legs and the method of braking.
The wings are broad and rounded, giving a
large safety factor. (From photograph by
Aymar.)

sharply between the downward and recovery strokes. The bastard
wing is held in such a position that the beat provides extra forward
momentum.

Landing is also a delicate operation, especially since it often involves
coming to rest suddenly on a branch (Fig. 276). This is achieved by
lowering and fanning out the tail, which thus acts as a flap, providing
both lift and braking. The legs are then lowered; often one further
wing stroke is given to bring the bird forward to drop onto the perch.
The adjustment of braking in such a way as to prevent stalling involves
a very special system of coordination (Fig. 277). Other methods of

464 THE BIRDS xvi. 19-

landing are possible, for instance, rooks may make a roll and sideslip
to the ground.

20. The skull in birds

The arrangement of the parts of the bird's skull is similar to that of
archosaurian reptiles (Fig. 242). Individual bones can be recognized
in the young, but they mostly become united in the adult to form a
continuous thin-walled structure that encloses the brain and sense-
organs and supports the beak (Fig. 278). Most birds are microsmatic;
the nasal passages are simple and the turbinals reduced. There is
seldom a complete bony secondary palate, such as there is in mammals,
instead the internal nostril opens into the mouth relatively far forward.
The large size of the brain and reduction of its olfactory portions are
responsible for the rounded form of the top of the head, and there are
very large orbits at the sides, separated by an ossified septum. The
base of the skull is formed by a basioccipital behind, carrying a single
occipital condyle. There is a large basisphenoid, covered ventrally by
a pair of basitemporals, probably representing the parasphenoid, the
front part of which makes a 'basisphenoid rostrum', as in archosaurs.

The jaws are characteristically slender and elongated; in the more
advanced birds they have a very special form of support. The upper
part of the front of the skull is composed of the enlarged premaxillae,
the nostrils lying very far back and the nasal bones being small. The
palatines are long and fused far forward with the maxilla, while they
articulate movably behind with the pterygoids and base of the skull.
The pterygoid is a slender rod, itself movably articulated with the
skull and with the quadrate, which is a triangular bone with clearly
separate otic and basal articular processes. The upper jaw is thus a
long thin bar composed of maxillae, quadrato-jugal, and jugal, and as
in many reptiles it is capable of considerable movement ('kinesis').
It is raised when the lower end of the quadrate moves forwards. This
mechanism is particularly well developed in parrots, where the beak
is freely hinged on the skull. This type of palatal arrangement is known
as neognathous. In some birds, such as the flightless ratites, the
palatines are shorter, the vomer larger, and the pterygoids less mov-
able, a condition called palaeognathous (p. 514). The lower jaw, also
elongated, consists of the articular bone and four membrane bones.

21. The jaws, beak, and feeding mechanisms

There is a complete lower temporal bar, composed of jugal and
quadrato-jugal bones. The temporal region is hard to interpret, but

XVI. 21

JAWS

465

Fig. 278. Skull of young gosling (Anser).
A. angular; Ar. articular; As. alisphenoid; Bo. basioccipital; Bsh. basisphenoid ; D. dentary;
E. ethmoid; Eo. exoccipital; F. frontal; Ip. interparietal; J. jugal; L. lachrymal; Mx.
maxillary; A r . nasal; O. supra-occipital; Op. opisthotic; P. parietal; Pa. palatine; Pm. pre-
maxillary; Po. postorbital; Pt. pterygoid; Q. quadrate; Qj. quadrato-jugal; R. rostrum of
basisphenoid; S. squamosal; Sa. sur-angular; V. vomer. (From Heilmann, The Origin of
Birds, H. F. & C. Witherby, Ltd.)

has presumably been derived from the diapsid archosaurian condition.
Typically, there is a single large fossa, communicating with the orbit,
but this is often partly subdivided by bony processes; occasionally,
there is a complete post-orbital bar (parrots). There are moderately
large temporal and pterygoid muscles, but the jaws are not usually

4 66

THE BIRDS

XVI. 21

Fig. 279. Various bird beaks.

1, Merganser; 2, Flamingo; 3, Shoveller; 4, Scissor-bill (adult); 5, Scissor-bill (young);
6, Anastomus; 7, Hornbill; 8, Hummingbird; 9, Avocet; 10, Parrot; 11, Parrot; 12, Spoon-
bill; 13, Crossbill; 14, Nightjar; 15, Eagle; 16, Balaeniceps. (From Pycraft, A History of
Birds, Methuen & Co., Ltd.)

very powerful, though, of course, formidable in carnivores. Having
completely lost the teeth, the birds must rely largely on internal
processes to break up the food. The beak is, however, characteristically
modified according to the food habits (Fig. 279). There is very great
variety in the feeding, as in so much of the life of birds, and though
many species keep strictly to one diet others are able to adapt them-
selves to the food available. The ingenuity and persistence with which
birds seek and collect food must be a main factor in their success.

Many birds with a moderately long bill, such as the song-thrush
(Turdus), can eat either flesh (snails, earthworms, or caterpillars) or

XVI. 21

BEAKS

467

fruit. Incidentally we may notice the ingenious behaviour by which
the snail's shell is cracked open to obtain the food, by beating it against
a stone. Birds that mainly eat seeds, such as the finches, usually have
short, thick, strong bills. Large strong bills are present in the hornbills
and toucans ; they push through dense foliage to obtain the fruit, which
may have a hard case. In parrots the beak is moved on the skull,
pushed up by the upper jaw when the latter is pulled forward by the
digastric muscle.

Fig. 280. The Galapagos woodpecker finch (Camarhynchus pallidus) using
its stick. (From Lack, drawn by R. Green from photograph by R. Leacock.)

The carnivorous birds, such as most eagles and owls, have short
and sharp beaks, whereas fish-eating, as in other vertebrates, results
in long jaws. Another widely found arrangement is the flattened bill
of some ducks, similar to those of some sturgeons and of the platypus,
which also sift out food from water or mud. The long, thin beak of the
curlew selects food from mud in a different way, mostly worms and
other soft-bodied invertebrates. Lesser flamingos feed on blue-green
algae and microscopic phytoplankton, collected by a filter system on
the jaws, using a current of water produced by the sucking mouth and
piston-like tongue. Some insectivorous birds have long beaks for
finding their prey under bark. The woodpeckers have a strong beak
like a pick-axe for excavating in wood, and most elaborate special
modifications for the purpose of licking up insects; there is an enor-
mously long protusible tongue and special hyoid. The woodpecker
finch {Camarhynchus pallidus) on the Galapagos Islands probes insects
from the bark by means of a cactus spine, a remarkable case of the use
of a tool by a bird (Fig. 280). Among the most specialized feeders are

4 68

THE BIRDS

XVI. 21-

the humming-birds, eating nectar, the beak being long or short accord-
ing to the type of flower visited, and the tongue provided with a
special tubular tip.

i net

22. Digestive system of
birds

Once the food is in the
mouth it is manipulated by
the long, thin tongue, mois-
tened with saliva, which
usually consists of mucus
but is said to contain diasta-
tic enzyme in some seed-
eating finches. Food swal-
lowed down the oesophagus
may be stored in a large
receptacle, the crop, found
especially in grain-eating
birds; its lining is of oeso-
phageal structure (Fig. 281).
The true stomach is divided
into two parts, a glandular
proventriculus and a muscu-
lar gizzard. The structure of
the anterior chambers of the
gut varies greatly with the
diet. In grain-eating birds,
such as the pigeon, the crop
is large and the seeds are
first macerated by storage
there. They are then mixed
with peptic enzymes in the proventriculus and ground up in the mus-
cular gizzard, which in pigeons has a horny lining and also contains
numerous small stones. In insectivores and carnivores the crop is
usually smaller or absent, but is very large in some fish-eating birds.
In carnivores the gizzard has the character of a more normal stomach.
It was stated by John Hunter that herring gulls, normally living on
fish, readily take to eating grain, and that after a year or so of this
diet the gizzard becomes muscular and has horny walls.

The peptic juice has powerful digestive powers and many carni-
vorous and fish-eating birds dissolve even the bones of their prey,

b.d

Fig. 281. Dissection of pigeon,
bile-ducts; cl. cloaca; coec. coeca; cr. crop; giz.
gizzard; int. intestine; k. kidney; /. liver; oes. oeso-
phagus; p. pancreas; p.d. pancreatic ducts; pr. pro-
ventriculus ; sp. spleen ; test, testis. (After Schimkewitsch
and Streseman.)

XVI. 22

ALIMENTARY CANAL

469

though in owls these are regurgitated with fur or feathers, making
characteristic pellets. The crop of pigeons is also remarkable for the
milk it produces to nourish the young. There are special glands for
this purpose and they become active in the breeding-season under
the influence of a pituitary hormone, prolactin, which has been

ur&vj

Fig. 282. Diagrammatic section through cloaca of pigeon.
ap. external aperture; b.Fab. bursa Fabricii; ep. epidermis; m.sph.
sphincter muscle; muc. mucous glands; r. rectum; ur, & vd. papillae
for ureter and vas deferens (or oviduct). (After Clara, from Streseman.)

crystallized and is probably protein in nature. Prolactin causes
regression of testes and ovaries and involution of secondary sexual
characters, but induces brooding behaviour in the female. Its action
is comparable with that of the galactogenic hormone of the mam-
malian pituitary.

The duodenum and coiled intestine are of characteristic vertebrate
tvpe, relatively rather short, though somewhat longer in grain-eating
birds. The bile and pancreatic ducts usually open into the distal limb
of the duodenum; in pigeons the left bile-duct enters close to the
pylorus (Fig. 281). There is a peculiar pair of coeca at the junction of
rectum and intestine. The food enters these coeca, but it is not clear
what function they perform, possibly it is related to the absorption of
water. The arrangements of the cloaca are certainly concerned with
this end (Fig. 282). The rectum opens into a coprodaeum and this in
turn receives a urodaeum, which is the terminal portion of the urinary
and genital ducts. A final chamber, the proctodaeum, opens at the
anus. The urinary products are made solid by subtraction of water in
the urodaeum and the walls of the other chambers serve a similar

47° THE BIRDS xvi. 22-

purpose. The bursa Fabricii is a blind sac with much lymphoid tissue,
opening into the proctodaeum; its function is probably to protect
locally against infection and to produce lymphocytes for the blood-
stream, hence it has been called a 'cloacal thymus'. Like the thymus,
it is prominent in young animals and usually much reduced in the
adult.

The large surface area, high temperature, and great activity of birds
necessitate a high food intake, especially in the smaller types. This is
made possible by rapid passage of food through the gut. Thus a shrike
(Lanius) is said to digest a mouse in 3 hours, and hens take only 12-24
hours over the most resistant grain. The amount of food taken per
day may reach nearly 30 per cent of the body weight (6 g) in the very
small goldcrest (Regains) but is about 12 per cent in a starling
(Sturnus) weighing 75 g.

23. Circulatory system

Many of the features characteristic of birds depend on an efficient
circulation, allowing of a high rate of metabolism, and hence a high
and constant temperature. It is significant that the birds and mammals
are the only vertebrates that have achieved complete separation of the
respiratory and systemic circulations, making possible a high arteriolar
pressure, which allows materials to reach the tissues rapidly.

The heart shows its sauropsidan characteristics clearly in that the
ventral aorta is split to its base into aortic and pulmonary trunks. The
former arising from the left ventricle curls round the pulmonary
trunk to form a single right aortic arch. The heart has lost the sinus
venosus; as in mammals no such extra chamber is necessary to step
up the venous return pressure. The ventricles are large, especially the
left. The right auricle and ventricle are separated by a flap-like valve,
the left side having valves with chordae tendinae, somewhat as in
mammals. There are enormous innominate arteries to supply the
pectoral muscles. In the venous system there are renal portal veins.

The size of the heart and rate of heart-beat vary with the size and
activity of the bird, larger birds having in general relatively smaller
and less rapid hearts. In a turkey the rate of beat may be less than 100
per minute, in a hen about 300, and in a sparrow nearly 500.

The red corpuscles of birds differ from those of mammals in being
oval and nucleated. They carry a large amount of a haemoglobin that
gives up its oxygen suddenly at a relatively high oxygen tension. The
red corpuscles are smaller in actively flying birds than in the larger
flightless ratites. Haemopoetic tissue is widespread in the young,

xvi. 24 R ESPI RAT ION 47 1

restricted mainly to the marrow in the adult, although it may also be
found in the liver and spleen. The white corpuscles are more numerous
than in mammals. They include neutrophils laden with crystals, and
thrombocytes, as well as the mammalian types. Lymphatic tissue is
dispersed rather than aggregated into nodes. There is a pair of lymph
hearts in the sacral region of the embryo and these may persist in the
adult. There is a high basal metabolic rate and a temperature con-
siderably higher than that of mammals, usually about 42 C, reaching
nearly 45 ° C in some cases. The means by which this is kept constant
in the absence of sweat glands are not known certainly. Heat loss is
minimized by the absence of vascularized extremities, the feet being
little more than keratin and collagen. The formation of the wing from
large avascular surfaces has no doubt been a large part of the secret
of the success of birds.

The air-sacs may serve to conserve heat by providing an air cushion
for the viscera, with perhaps the alternative possibility of losing heat
in this way, by ventilation, when necessary. There is a system of
direct arterio-venous connexions in the feet, and elsewhere. The anas-
tomotic regions have powerful muscles, whose contraction closes them
and forces the blood through the capillary system. There must be a
whole system of nervous pathways for the control of upward and down-
ward temperature regulation, evolved independently of that found in
mammals. At least one species (the nightjar) is known to hibernate,
and certain humming birds, whose small size render heat loss a
serious problem, become temporarily poikilothermic at night.

24. Respiration

Special arrangements are present to provide the large supply of
oxygen necessary for the active metabolism and these are based on the
plan found in some reptiles. Beyond the respiratory portion of the
lung, which is relatively small, there are membranous air-sacs, which
are filled at inspiration and then sweep the used air out of the lungs
at expiration, thus avoiding the 'dead space' of unrespired air, which
is considerable in mammals. When the bird is at rest the air-sacs con-
tain air with a high content of C0 2 , but during periods of activity the
abdominal air-sacs fill with fresh air containing little C0 2 ; they then
serve not only as a means of ventilating the lungs but also for regula-
tion of the body temperature. The exact direction of the air currents
passing through the lungs and the different air-sacs is not fully under-
stood.

The larynx of birds is a small structure guarding the entrance to the

472

THE BIRDS

XVI. 24

trachea. The latter is often long and coiled, perhaps to warm the air.
The tracheal rings are bony and complete. The voice is produced in
the syrinx, a slight enlargement at the lozver end of the trachea, con-
taining a pair of semilunar membranes with muscles that alter the
pitch of the sound. The apparatus is simple in many birds, but the
muscles are very complicated in the singing birds and are especially

s.cerv

s clav

s. thor
ant

s Lhorpost

s.abd.

Fig. 283. Diagram of lungs and air-sacs of pigeon, seen from ventral side on left,

dorsal on right. On the left side only the ventral surface of the lungs and the

expiratory bronchi and air-sacs are shown (dotted). On the right are the inspiratory

bronchi and air-sacs (in black).

B. main bronchus; C. cervical ventrobronchus; M. mesobronchus; V. vestibule; s.abd.

abdominal air-sac; s.cerv. cervical air-sac; s.clav. clavicular air-sac with diverticulum (ax.)

in axilla; s. thor. ant. and post, thoracic air-sacs. (After Brandes and Ihle.)

large in the males. Many varieties of sound are produced, from simple
cries appropriate to each sex to elaborate songs. In many species the
song is given in its full complexity by individuals that have had no
opportunity of hearing others sing, but in some the song is largely
learnt by the young and may show considerable local variation. The
voice is used for communication in various ways, including, in social
birds such as rooks, the giving of warning and the frightening away
of intruders. The language may include as many as fifteen sounds used
under different circumstances (chaffinch). The more elaborate song of
male birds is used in courtship both as a sexual stimulant and as a
threat to other birds invading the chosen territory (p. 503).

xvi. 24 RESPIRATION 473

The lungs are rather small spongy organs, with little elasticity. The
air passes backwards in a large main bronchus running through the
lungs and giving off branches to the lung substance, but continuing
beyond to the inspiratory air-sacs (Figs. 283 and 284). These are thin-
walled chambers, divided into two sets, the posterior inspiratory and
anterior expiratory. The posterior, inspiratory, air-sacs are the ab-
dominal and posterior thoracic and they
are filled by the air rushing into them
through the main bronchus. The anterior
or expiratory air-sacs include an anterior
thoracic, median interclavicular, and cer-
vical, these often communicating with
spaces in the bones. At expiration the
air passes from the more posterior sacs
through the lungs by special recurrent
bronchi into the anterior sacs. From
these the air may be expelled to the
exterior, return to the lungs being pre-
vented by closure of sphincters. In some
conditions, however, especially in diving
birds, the air may be passed backwards
and forwards through the lungs several
times, until all its oxygen has been used.
The branches of the bronchi in the lungs
do not end blindly in alveoli, but make an
elaborate system of lung capillaries. Air
sweeps through the larger channels at
inspiration and expiration, but probably
reaches the finer capillaries by diffusion.

The mechanism by which the ventilation is produced is complicated
and depends largely on the movements produced during locomotion.
The upper surface of the lung adheres to the ribs, its lower surface is
covered by a special membrane derived from the peritoneum and
known as the pulmonary aponeurosis (Fig. 285). This is connected
with the ribs by costopulmonary muscles. The floor of the thoracic
air-sacs, which lie below the lungs, is also covered by a fibrous mem-
brane, the oblique septum, but the walls of the remaining air-sacs are
very thin. Quiet respiratory movements are produced by the inter-
costal (inspiratory) and abdominal (expiratory) muscles, acting upon
the thoracic and abdominal cavities so as to enlarge and contract the
thorax, drawing air in and out of the air-sacs, through the lungs. During

Fig. 284. The air-sacs of a bird.

1.. right lung; c. cervical air-sac; ICL.
interclavicular; A.S. outgrowth into
humerus (h.); A.th. anterior thoracic
air-sac; p.TH. posterior thoracic;
AnD. abdominal air-sac; tr. trachea.
(From Thompson, Biology of Birds,
Sidgwick & Jackson, Ltd.)

474 THE BIRDS xvi. 24-

flight the movements of the pectoral muscles provide the ventilation,
the sternum moving towards and away from the vertebral column.

25. Excretory system

The kidneys are, of course, metanephric and are relatively large,
elongated, and lobulated. They are provided with venous blood by

-thas

obi--

rpr

ms /

Fig. 285. Diagram of transverse section through the thorax of a bird.

ec. Excurrent passage from lung to air-sac through pulmonary aponeurosis; h. heart;
lis. left liver-sac; Ig. lung; m. muscle; ms. mesentery below oesophagus; obi. oblique septum;
p. pericardial coelom; pa. pulmonary aponeurosis; pic. reduced pleural coelom; r. dorsal
rib; re. recurrent bronchus from sac to lung; rl. right lobe of liver; rpr. right pulmonary
recess; St. sternum; thas. posterior thoracic air-sac; vr. sternal rib. (From Goodrich.)

the renal portal veins and arterial blood from the renal arteries. The
arrangement is essentially as in amphibia and reptiles, with the renal
arteries supplying the glomeruli and the portal veins, which break up
into inter-lobular branches, sending blood to the renal tubules, whence
it is collected into a central intra-lobular vein. It is not certain, how-
ever, exactly how the system operates, and it is possible that much of
the blood-flow is directly from the renal portal to the renal veins,
making little contact with the tubule walls.

The excretory system is highly specialized for water-saving. For
this purpose the end product of nitrogenous metabolism is the rela-
tively insoluble uric acid, synthesized in the liver, probably from
ammonium lactate. After excretion by the kidney the urine is con-
centrated in the cloacal chambers and the uric acid precipitates as

XVI. 26

REPRODUCTION

475

whitish granules. There is no urinary bladder in the adult bird. More
soluble excretory end substances, such as urea, would reach toxic con-
centrations. The glomeruli are much more numerous and smaller
than those of mammals. The urinary tubules effect a considerable con-
centration of the urine by means of long loops of Henle. The viscous
fluid that enters the urodaeum then
passes up into the coprodaeum,
where further water is abstracted,
and the mixed faeces and urinary
products are then excreted as the
characteristic semi-solid white
guano. The water-conservation sys-
tem is certainly very effective, and
some desert-living birds are said to
be able to survive for many weeks
without water. In this respect the
birds have freed themselves from
the original aquatic environment to
a remarkable degree.

RR.OVD
OPUR

OPOVD
CL

Fig. 286. Female reproductive organs
of a hen.

ov. ovary; K. kidneys; f.t. funnel; ovd.
oviduct; m.ovd. muscular part of oviduct;
OP. OVD. opening of oviduct; ur. ureters;
op.ur. opening of right ureter; r.r.ovd.
rudimentary right oviduct; cl. cloaca. (From
Thompson, Biology of Birds, Sidgwick &
Jackson, Ltd.)

26. Reproductive system

The testis consists of coiled
tubules of the usual type, joining to
form a long epididymis and vas
deferens, opening into the urodaeum
by an erectile papilla that is the only
copulatory organ of most birds.
During copulation the proctodaea
of male and female are everted and
pressed together, so that the sperm
is ejaculated direct into the female urodaeum and finds its way up
the oviduct. A definite penis (and also clitoris) is found in ratites,
anseriformes, and a few other birds. The condition of the testis and
its ducts varies greatly with the time of year, the weight of the gland
being as much as 1,000 times greater in the breeding-season than it is
in the non-breeding, when it contains only spermatogonia.

The provision of material sufficient for the development of a warm-
blooded creature is, of course, made possible in birds by the extremely
yolky eggs, so large that they allow room for development of only one
ovary, nearly always the left (Fig. 286). The right ovary remains present
as a rudiment and if the left is destroyed by operation or disease the

476

THE BIRDS

xvi. 26-

right is able to differentiate, but then forms not an ovary but a testis.
Complete sex reversal can thus occur, at least in some races of
domestic fowl, and the transformed bird may acquire cock plumage
and tread and fertilize hens (Fig. 287). Sex reversal rarely, if ever,
takes place in the opposite direction. We must suppose that there is
some switch over in the balance of male and female determining

Fig. 287. Secondary sexual characters of the fowl (Gallus).

Left cocks, right hens.

A, normal; B, castrated; C, cock with implanted ovary and hen

with implanted testis. (After Zawadowsky.)

processes, taking place relatively early in the case of normal definitive
males but later on in life also in 'females', so that all birds become
potentially 'male' at the end of their life.

Of the large number of oocytes only few ripen to make the enormous
follicles. After each follicle has burst it quickly regresses; there is no
'corpus luteum'.

The egg is taken up by the ciliated and muscular funnel of the left
oviduct, and passes down a tube with circular and longitudinal muscles
and a glandular, ciliated mucosa. The albumen of the egg is produced
by long tubular glands, opening to the lumen. The oviduct has various

xvi. 27 BRAIN 477

parts, the upper secreting mainly albumen, the lower producing the
shell, and the lowest mucus, to assist the act of laying. The blue back-
ground colour of the egg (oocyanin) is produced during shell-forma-
tion in the upper part of the tube ; spots of red-brown ooporphyrin are
added lower down. The pigments are derived from the bile, ultimately
from haemoglobin.

As much as a third of the weight of calcium in the whole skeleton
is needed for the shells of the two eggs laid by a pigeon. A reserve is
collected as the ovarian follicles mature. The oestrogen they produce
increases the uptake of calcium from the food and stimulates its
deposition in the bones. After ovulation the oestrogen level falls, the
calcium is mobilized from the bones, and its concentration in the
blood becomes very high, until used by the eggs.

27. The brain of birds

The brain is larger relative to the body in birds than in any other
vertebrates except mammals (Fig. 288), and there is no doubt that one
result of the high temperature has been to allow opportunity for an
elaborate nervous organization and complicated behaviour. Unfortu-
nately we have little information about the w^ay in which the large
masses of tissue of the brain function ; they are certainly different from
anything found in mammals. There are considerable differences in the
development of the parts in various birds, for instance, the forebrain is
especially large in the rooks and crows (Corvus) and in the parrots, the
behaviour of which also shows signs of outstanding 'intelligence'.

In the spinal cord the most characteristic feature is the relatively
small size of the dorsal funiculi, and their nuclei in the medulla are
also small. Evidently the sense of touch is less well developed over the
body than it is in mammals, perhaps less than in reptiles. No doubt
movement of the feathers provides impulses leading to reflex actions,
but it is not surprising that the loose covering does not allow elaborate
organization of the sense of touch. The finer senses of birds are
restricted to the eyes, ears, and bill. On the other hand, there are large
spino-cerebellar tracts, presumably proprioceptive and concerned with
the delicate adjustments necessary for flight. The spinal cord is con-
trolled by large efferent tracts from the brain, including cerebello-
spinal, vestibulo-spinal, and tecto-spinal pathways. There is no direct
tract from the forebrain to the spinal cord, but the influence of the
large corpora striata is probably exercised through fibres running to
the red nucleus and tegmentum of the midbrain, from which others
pass to the cord.

478

THE BIRDS

xvi. 27

XII
IX,X,XI
Vllanc/VIII

The cerebellum is also large (Fig. 288), a state of affairs perhaps
connected with the precise timing and control of movement in all
planes of space during flight. Besides large spino-cerebellar and
vestibulo-cerebellar pathways there are also tecto-cerebellar and
strio-cerebellar tracts, the latter perhaps conducting in both directions.
The effect of the cerebellum on other parts of the brain is exercised
through cerebellar nuclei, the cells of which give origin to the cerebello-
spinal tract.

The optic tracts are completely
crossed and end mainly in the
midbrain, as in lower verte-
brates. However, a considerable
portion of the optic tracts passes
to the thalamus, and the mid-
brain and thalamus are both
highly developed and have inti-
mate and reciprocal connexions
with the striata of the cerebral
hemispheres. The optic lobes
also receive ascending fibres from
the trigeminal nuclei and from
the spinal cord. Their efferent
pathways run to the oculomotor
nuclei, to the underlying teg-
mentum, and to the medulla and
spinal cord. Evidently they play
a large part in correlating visual with other afferent impulses. The
thalamus is large and its dorsal part well differentiated into nuclei.
It receives, besides optic fibres, also projections from tactile, pain,
temperature, and perhaps auditory sources. There are large thalamo-
striatal tracts, probably conducting in both directions. The ventral
thalamus receives impulses from the striatum and sends them to the
tegmentum, this being the main efferent pathway of the forebrain.
The hypothalamus is rather small, probably because of the reduction
in the olfactory system.

The cerebral hemispheres are much larger than any other part of the
brain and show an exaggeration of the condition found in the lizards
(Fig. 289). The ventro-lateral portions are enormously developed,
whereas the medial ventral walls are thin and the pallium is quite
small, thin, and not folded. The olfactory regions of the brain are
small, including the hippocampus.

Fig. 288. Brain of a duck (Anser)

c.h. cerebral hemisphere; cereb. cerebellum; cp.

epiphysis;/?, flocculus; h. hypophysis; o./. optic

lobe; olf. olfactory lobe; str. striatum; 1I-XII,

cranial nerves. (After Butschli and Ihle.)

XVI. 28

FUNCTION OF BRAIN

479

The corpus striatum is a huge solid mass of tissue, receiving projec-
tions forward from the thalamus and sending them back through the
latter, to the midbrain roof and floor, to the cerebellum, and thence to
the medulla and spinal cord. This very characteristic striatum can be
divided into various regions. The part representing the 'original' or
lower striatum is called the 'paleostriatum' ; other parts, lying above
this, are known as the mesostriatum and hyperstriatum.

Fig. 289. Transverse section through forebrain of sparrow.

hip. hippocampus; hyp.str. hyperstriatum; mes.str. mesostriatum; n.pr. preoptic nucleus;
pal.str. palaeostriatum; pall, pallium. (Partly after Kappers, Huber, and Crosby.)

28. Functioning of the brain in birds

Loss of one complete hemisphere by a pigeon is not followed by any
gross motor defect or asymmetry of movement. This suggests that the
corpora striata do not control individual muscle movements, which
agrees with the fact that there is no direct pathway from the forebrain
to the spinal cord, corresponding to the pyramidal tract of the mam-
mals. Electrical stimulation does not produce movements; the striata
are 'silent areas' to stimulation.

Complete removal of both hemispheres does not reduce a pigeon to
a helpless state. The animal can still maintain its temperature and its
balance and can feed itself if the food is placed near to it. However, a
bird so treated is far from normal. It may show a lack of activity,
remaining inert for long periods, and then become aimlessly restless
for a while. Evidently the normal balance of excitation and inhibition
has been upset. Deficiencies in vision can be detected in birds with
various portions of the cerebral hemispheres removed, and the mating
and nestine behaviour are also affected. Even small removals of the

480 THE BIRDS xvi. 28

cortex and top of the striatum are said to prevent incubation (though
not copulation) and with deeper lesions the whole process of rearing
the young becomes impossible.

These observations on the functions of the brain of pigeons may not
be applicable to birds in general. The forebrain is larger in many other
birds than in the pigeon, and there is some evidence that in the parrots
movements and even 'phonation' can be elicited by electrical stimula-
tion of the corpora striata, which are especially large. Removal of one
particular area is said to lead to disturbances of 'speech'.

Fig. 290. A. Models used by Lorenz and Tinbergen. Small birds reacted with

escape movements to the models marked + . B. The model induced escape reactions

when towed to the right ('hawk') but not when towed to left ('goose').

(From Tinbergen.)

It seems, therefore, that the large masses of nerve-cells in the striata
are concerned in some way with the elaboration of the more complex
acts of behaviour. This is a very vague statement, but is the best that
we can give at present. It may be that further investigation of the
reciprocal actions of striatum and thalamus will show whether the
essentials of their action consist in some reverberating or scanning
systems and whether these actions are at all similar to those in the
forebrain of mammals. The fact that the striatum consists of solid
masses of tissue suggests that the arrangement does not depend, as
does the mammalian cerebral cortex, on the projection of patterns of
excitation onto an extended surface.

Birds are usually said to show more stereotyped patterns of instinc-
tive behaviour than primitive mammals. Once they have embarked on
a line of action, even a complex one like nest-building> they are sup-
posed to pursue it in a given manner, without ability 10 adapt them-
selves to unusual happenings. Watching the exploratory behaviour of
a robin or a tit it is difficult to feel that the existence of this difference

xvi. 28 BEHAVIOUR 481

is adequately proved, but whatever distinction exists is presumably a
reflection of the difference between the functions of large masses and
spread-out sheets of nervous tissue. Certainly birds can count as well
as rodents, and their performance in mazes and puzzle boxes is at
least comparable to that of most mammals.

There are many signs that a suitable initial stimulus sets off in the
bird a whole train of behaviour, organized from within. On the other
hand, inappropriate stimuli may sometimes set off a reaction, as if the
'keys' to these cerebral 'locks' were not very elaborate or specific. A

Fig. 291. Pintail ducks (Anas acuta). Males displaying dark brown feathers
of neck with white bands on either side. (From Tinbergen, after Lorenz.)

robin held in the hand may burst into song, cock ostriches frightened
by an aeroplane fall to the ground in their characteristic sexual display.
Birds frightened or disturbed may proceed to the actions of bathing,
preening, feeding, or drinking, performed in a ritual and cursory
manner for a long time. Such displacement activities show that the
organization of the bird's nervous system, like that of a mammal, pro-
vides for some strange deviations, whose study may reveal much about
the method of working of the brain.

Many complex forms of behaviour are responses to only limited
parts of the natural stimulus situation. Thus when the models shown
in Fig. 290 were towed above certain young birds, only the models
marked with a cross induced escape reactions: apparently the con-
figuration of the short neck is the essential feature. Much of the
elaborate social life of birds depends on such sign stimuli displayed
by one bird (the 'actor') and serving as releasers setting off particular
actions or trains of action in another bird (the 'reactor'). Many of the
elaborate forms of display evolved by birds (p. 497) are releasers of
this sort (Fig. 291), and structures and actions on the part of the
young release the appropriate behaviour of the parent. The red breast

482 THE BIRDS xvi. 28-

of the robin (Erithacus) is the agent that releases attacks by other birds
(Fig. 292). Similar phenomena are known in fishes and other verte-
brates (p. 225), and it remains to be shown whether they can be attri-
buted to any single or particular neural basis.

29. The eyes of birds

Birds depend more on their eyes than on the other senses; they are
perhaps more fully visual than are any other animals. The eyes are
extremely large : those of hawks and owls, for instance, may be abso-
lutely larger than in man. The shape is not spherical, the lens and

Fig. 292. The red tuft of feathers is attacked by male robins holding territory, but
the complete juvenile bird (withou red) is left alone. (After Lack, from Tinbergen.)

cornea bulge forwards in front of the posterior chamber, this form
being maintained by a ring of bony sclerotic plates (Fig. 293). In most
birds the whole eye is thus broader than it is deep, but in those with
very acute sight it is longer, and in some eagles and crows becomes
almost tubular. The great distance between lens and retina allows
broadening of the image, thus improving the fine two-point discrimin-
ation that is needed by these diurnal birds. The shape of the back of
the eye is such that 'the retina lies almost wholly in the image plane,
so that all distant objects within the visual angle are sharply focused
on the photosensitive cells, whereas in the human eye this is only
true of objects lying close to the optic axis' (Pumphrey; Fig. 294).
The lens is usually soft and accommodation is effected by changing
its shape, and especially the curvature of its anterior surface, by the
pressure upon it of the ciliary muscles behind. These, like the iris
muscles, are striated, presumably allowing for the quick accommoda-
tion necessary in a rapidly moving bird, though it must not be for-
gotten that these muscles are also striated in lizards. The ciliary
muscle is characteristically divided into 'anterior' and 'posterior' por-
tions, the muscles of Crampton and Briicke (Fig. 293). The latter
draws the lens forward into the anterior chamber so that since the

ACCOMMODATION

XVI. 29 A^V^UiVli\lUJL»/\ 1 IKJ1S 483

shape of the eye is fixed by the sclerotic plates, the lens becomes more
curved and hence accommodated for near vision; contraction of the iris
sphincter assists in the process. Crampton's muscle is so arranged as
to pull on the cornea, shortening its radius and further assisting in

lb)

(3)

tenacular Ligament: v / /
Cramp tons m. \/'

scleral ossicle

lens

Bruckes m.

cdiary
body

zonule

Fig. 293. The mechanism of accommodation in a bird's eye;

the positions during near vision are shown dotted, b. The lens of

the cormorant's eye at rest (full line) and fully accommodated

(dotted line). (From Pumphrey, after Franz and Hess.)

■cornea-

scleral ossicle

pecten

Fig. 294. Diagrams of right eye of man and left eye of swan to show the difference
in shape. The position of the image plane in man is shown dotted; it lies behind
the retina except near the centre. The arrows point forward. (From Pumphrey.)

accommodation. This double method of active accommodation for
near vision is most fully developed in diurnal predators, such as the
hawks, less so in night-birds. In aquatic birds Crampton's muscle is
reduced, and the cornea is of little importance in image-formation.
Special arrangements are found in diving birds, for instance in the
cormorants Briicke's muscle is large and there is a very powerful iris
muscle, which assists the ciliary muscles to give the great change in
shape of the soft lens, allowing accommodation of 40-50 diopters (about

4«4 THE BIRDS xvi. 29

10 in man). The kingfishers are said to possess an amazing arrangement
of double foveas, placed at different distances from the lens, so that
as the bird dives under water the image is transferred from one fovea
to the other without any change in the dioptric apparatus. These details

Herring Gull
(Larus)

Shearwater
r Puffinus)

Great: Bustard
(Otis)

Coot
(Fulica)

Ostrich
(Struthio)

Cormorant
(Phalacrocorax)

Humming Bird
fCalypte)

Shrike
fLanius)

King Fisher
(filcedo)

Fig. 295. The appearance of the retina of various birds as seen with an

ophthalmoscope through the pupil.

cm. central area;/, fovea; p. pecten; t.a. temporal area. (After Wood, from Pumphrey.)

of the visual system show, like so many other features of bird ana-
tomy, how readily the structure conforms to special habits of life.

The retina of day-birds consists largely but not wholly of cones;
these animals are more fully diurnal than is man. The high resolving
power and hence high powers of discrimination and of movement-
detection depend on the great density of the cones, as many as
1 million to each square millimetre in the fovea of a hawk, three times
denser than in man. Nocturnal birds, on the other hand, have retinas
composed mainly or completely of rods, and the differences between
the behaviour of these two types of eye, found in birds as in mammals,
have been a powerful support for the duplicity theory of vision. There
are usually one or more areae, regions of the retina consisting of tightly

xvi. 29 RETINA 485

packed receptors. In birds that live on the sea, in the desert, or other
open spaces the area often has the form of an elongated horizontal band
(Fig. 295), whereas in tree-living birds it is circular. Some birds have
two areae, a central one in the optic axis and a second placed on the
temporal surface of the eye, so that the image of objects in front of the
head falls on the temporal areae of both eyes. This arrangement is
common in birds that follow moving prey (shrike, Lanius) or for

Fish (Serrjnus)

fovea
(dFcer Kahmjnn)

Reptile [Chameleon)

Fovea
(aFter Detwiler)

uila \ X Aquila

central fa ea \ temporal Fovea

(after Polijak) \ (after Pol yak)

Alcedo
central fovea
(after Kolmerj "<~

(after Detwiler)

Fig. 296. Forms of the fovea in various vertebrates, showing
the development from moderately to sharply convexiclivate types
in foveas adapted for detection of movement, but flattening of
the fovea where there is binocular vision. (From Pumphrey.)

some other reason require accurate perception of distance (swallows,
humming-birds; the latter feed their young on insects caught on the
wing). The density of the cones is so high in diurnal birds, even outside
the areae, that they probably obtain a good detailed picture in all
directions. They do not, therefore, scan the world with the central
area of the retina as we do; indeed, the eyes move relatively little.
Instead the bird is able to detect very small movements anywhere in
its surroundings. The bird's-eye view usually lacks stereoscopic solidity
and it is possible that in compensation for this the animals appreciate
distance by movements of the intrinsic eye-muscles. The familiar
cocking of the head of a bird before pecking may be its means of
judging distance.

As in man there is often within the central area of the eye a fovea
or pit, and in many birds the sides of this pit are steeply curved (Fig.
296). Walls has suggested that since the vitreous humour and retina
differ in refractive index this curvature serves to magnify the image

486 THE BIRDS xvi. 29

and increase acuity. Pumphrey points out that any such advantage
would be counteracted by the aberration introduced and he makes the
suggestion that this disturbance of the picture by the 'convexiclivate'

Fig. 297. Effect of refraction produced by the curvature of the fovea
of the golden eagle. An image of the form shown with dotted lines is
distorted by the fovea to the form shown in solid lines. The circle
represents a radius of io/j. at the centre of the fovea. (From Pumphrey.)

Fig. 298. Distortion by the fovea. The lines represent the successive images at
equal time-intervals of the boundary of a regular object when the object moves
steadily across the visual field. If this picture is viewed at 7 m the area of irregu-
larity subtends an angle about equal to the angle subtended by the central part of
the hawk fovea. It will be found that the irregularity is very evident to the human
eye at this distance though the lines are resolvable with difficulty.
(From Pumphrey.)

fovea is itself an advantage, improving the power of fixation and sensi-
tivity to movement, at the sacrifice of acuity. Such an arrangement
would serve to emphasize angular displacements, transforming a
radially symmetrical image into an asymmetrical one, except when
there is coincidence between the axes of symmetry of the fovea and of

xvi. 29 COLOUR DISCRIMINATION 487

the object (Figs. 297 and 298). Foveas with steep sides are found in
birds of prey, kingfishers, and others that have very high powers of
detecting movement; a similar but less pronounced arrangement is
found in fishes and reptiles. It is probable that the primitive functions
of the eyes were fixation and detection of movement, rather than reso-
lution of detail and recognition of patterns. Some birds have one con-
vexiclivate and one flatter fovea (Figs. 295 and 296), the latter being on
the temporal surface of the retina and used in binocular vision. The
fovea is also flat in the retinae of primates with binocular vision; evi-
dently the optical errors of a curved fovea cannot be tolerated where
there is fusion of the two retinal images.

Birds undoubtedly discriminate colours, apparently on a trichro-
matic basis similar to that of mammals. No other animals, except
perhaps primates, show such responsiveness to colour in their
surroundings, including the food and other members of the species.
In animals that move so freely recognition and attraction of the sexes
is more efficiently performed in this way than by touch or odour.
The cones of birds often contain red and yellow droplets, which may
heighten visual acuity by reducing the effects of chromatic aberration.
The droplets in the central area are always yellow. The presence of
droplets of various colours in adjacent cones may also increase powers
of discrimination. Sometimes the droplets are so arranged as to allow
accentuation of different contrasts in the parts of the visual field. The
lower part of the pigeon's retina contains red, the upper yellow filters,
increasing the contrast of blues and greens respectively, as required
for vision against the sky in the one case and the ground in the other.
There have been many investigations of the distribution of sensitivity
in the retina; probably many birds are rather insensitive to the blue
end of the spectrum. There is no truth in the suggestion that the eyes
are sensitive to infra-red radiation.

Although the eyes of some birds are directed forwards, so that their
fields overlap, they are said not to have binocular vision and decussa-
tion of the optic tracts is complete. Perception of distance, a very
important function for the bird, must be performed in some other
manner. In many birds the eyes are directed sideways, and the fields
of view may even overlap behind the head, for example in waders.
This may serve to give warning of predators. Many functions have
been suggested for the most enigmatic organ of the bird's eye, the
pecten, a pleated highly vascular fold, projecting from the retina into
the vitreous. It is possible that the irregular shadow cast by this organ
provides, as it were, numerous small blind spots and hence by a

4«S

THE BIRDS

xvi. 29-

stroboscopic action increases the number of on-and-off effects pro-
duced by a small object in the visual field, increasing contrast and
allowing detection of its movement. This, however, is only one of the
numerous suggestions about the function of the pecten, and the only
real support for the idea is that the body is large and much pleated in
predatory birds, which detect minute movements at great distances,

Fig. 299. Tracing of the shadow of the pecten on the retina
in various birds. (After Pumphrey and Menner.)

and is small and smooth in nocturnal birds (Fig. 299). However, it is
almost certain that the original function of the pecten was to bring
nourishment to the vitreous and retina. It has often been suggested
that the pecten is in some way connected with accommodation; it is
not likely that it actually assists in focusing, for instance, by pressing
forward the lens, and no changes have been seen in it during accom-
modation. However, it might possibly assist by adjusting the intra-
ocular pressure, which must be increased by the extensive changes in
the lens during accommodation.

30. The ear of birds

Both vestibular and auditory parts of the ear are well developed in
birds. The former are not known to possess special peculiarities, but
the large connexions with the cerebellum suggest great importance in
the operations of flight, presumably especially by the semicircular
canals. There is a distinct cochlea, slightly curved and especially well

xvi. 30 EAR 489

developed in owls and in parrots (Fig. 300). In this there is a basilar
membrane, with fibres increasing in length towards the tip and carry-
ing an organ of Corti with hair-cells in contact with a tectorial mem-
brane (Fig. 301), as in mammals. At the tip of the cochlea is a special
sensory region, the lagena, similar to that of lower vertebrates and
perhaps responsible for reaction to lower notes, the basilar membrane

Bind

Mammal

Fig. 300. Labyrinths of various vertebrates, to show

varying development of cochlea (c) and lagena (l).

s, saccule; u. utricle. (From v. Frisch.)

responding to the higher frequencies. Birds are known to be more
sensitive to distant gunfire and other low-frequency vibrations than is
man. Transmission of vibration from the tympanum to the inner ear
is effected by the columella auris, derived from the cartilages of the
hyoid arch. The inner portion of the columella is rod-like (stapes), but
the outer end makes contact with the tympanum by means of three
processes, of somewhat irregular shape.

Hearing is, of course, acute and the song-birds must be able to dis-
criminate between simple tunes; some of them are surprisingly good
mimics. Ability to localize sound is high and owls and other night-
birds probably find their prey largely by ear. For the purpose of
direction-finding they have developed an asymmetrical arrangement
of the ear cavities (Strix) or asymmetrical external ears (Asio). A few
birds that live in caves have the power of avoiding obstacles by echo-
location (Steatornis, the oil bird, Collocalia, swiftlet). They emit up
to 5 to 6 clicks a second at 4 to 5 Kc. The rate varies inversely with
the amount of light and increases when obstacles are met.

4QO

THE BIRDS

xvi. 31

31. Other receptors

The corpuscles of Grandry in the bill of ducks and other birds are
probably touch receptors, comparable to Meissner's corpuscles in
mammals. The corpuscles of Herbst, found in the dermis elsewhere in

Fig. 301. a. Diagram of section of bird's ear.

b.m. basilar membrane; col. columella; ex. extra-columella; E.t. Eustachian tube;

f.r. round window; h.c.C. hair-cells of Corti's organ; h.c.l. hair-cells of lagena; sacc.

sacculus; s.t. scala tympani; s.v. scala vestibuli; t.m. tectorial membrane; t.v. tegmentum

vasculosum; tym. tympanic membrane.

b. Diagram of section across cochlea of a bird.
G.cochl. cochlear ganglion; s.m. scala media; other lettering as in A. (From Pumphrey,

after Satoh.)

the body, resemble Pacinian corpuscles. They may be receptors for
vibration and are numerous in certain situations, for example in the
feather follicles, the beak, between the tibia and fibula, and in the tip
of the tongue of a woodpecker.

Chemoreceptors for taste and smell are little developed. There are
few taste-buds on the tongue. The nasal cavity is large but the
olfactory epithelium restricted. It is doubtful whether most birds use
the nose as a distance receptor; they may use it to test air coming from
the internal nostril. In kiwis, however, which are nocturnal and terres-
trial, the olfactory sense is well developed.

XVII

BIRD BEHAVIOUR

1 . Habitat selection

The success of bird life has been largely due to the great variety and
ingenuity displayed in finding situations suitable for providing food
and allowing reproduction. Their powers of habitat selection allow
diversification of species by reducing interspecific competition. Species
living in the same area rarely eat the same food, especially if it is
scarce. It is often said that birds are creatures of stereotyped habits,
yet they have certainly exploited their mobility to the full; they obtain
the means of life in most various ways. This mobility makes it difficult
to specify the 'environment' of a bird. For instance, a swallow may
pass part of its life in the tropics, part near the Arctic Circle. A gull
may nest on a rock, eat grain in a field, and then fish in the sea, all
within a few hours. Observation of the familiar birds of town and
country soon shows that they are at home in a much greater variety
of situations than could be supported by most animals, and that within
limits they can adapt their behaviour to each situation. Birds show,
therefore, in a marked degree, two of the features most commonly used
as criteria for the recognition of a higher animal, namely, freedom to
move to different conditions and ability to obtain a living in unpromis-
ing circumstances.

Nevertheless each species nests in a limited variety of habitats and
feeds in a limited variety of habitats. There is evidence that the
appropriate habitat is recognized by a relatively small number of
conspicuous features, independently of learning.

2. Food selection

Where the food is very specific substitutes will only be accepted
under unusual conditions of starvation, but many birds are more
catholic in tastes and some of these are among the most common, for
instance rooks, starlings, thrushes, blackbirds, and gulls. Both field
observation and experiment suggest that birds quickly learn from
experience where and how food may be obtained. They will remember
to visit an abundant source of supply and there are numerous stories
of the ingenuity of such birds as the jackdaws in obtaining it. This
short-term memory is probably of great importance in allowing the

492 BIRD BEHAVIOUR xvn. 2-

bird to establish an effective routine for each part of its life, especially
as it is combined with the power to explore elsewhere when conditions
change.

Food selection thus depends on species-characteristic motor patterns
and structures, whose use varies to suit the circumstances. There is an
initial responsiveness to a wide range of stimuli, later modified by
learning. In young birds these actions are not necessarily related to
appropriate objects or situations. Thus young chaffinches or tits peck
at spots of many sizes, but only when they are not hungry. When they
are, they beg from the parents. Young kestrels 'play' at hunting pine
cones, even after obtaining food by real hunting (see Hinde, 1959).

This range of response is then narrowed by learning. Objects that
provide food are pecked again, those that do not or are distasteful are
avoided. The range of learning that is possible must, however, be
influenced by the hereditary equipment. Thus chaffinches never use
the foot to hold objects but goldfinches and tits do so and can thus
learn to pull over a grass stem and peck off insects otherwise out of
reach, or indeed to open milk bottles!

3. Recognition and social behaviour

Great mobility has made it necessary for birds to develop specific
means for recognizing their fellows, their enemies, and their com-
petitors; from this power an elaborate social life has developed in
many species. In spite of their freedom many birds are not indivi-
dualists, they live much of their lives together in flocks; the unit of
life is larger than the 'individual' body. Species feeding on the ground,
such as rooks, starlings, and partridges, commonly move about in
groups during the winter and obtain the advantage that the alertness
of each single bird serves to warn for many. The lack of procryptic
coloration in some of these social birds is a measure of the effectiveness
of the protection afforded by the society; indeed, it may be advanta-
geous that the birds should be conspicuous to their fellows. Starlings
carry the communal life farther by collecting together in large numbers
each night to roost. As many as 100,000 may be found in one roost,
the birds flying home from their feeding-grounds every night for
distances of many miles. Possibly in this way the disadvantage of the
conspicuous outline is minimized while roosting. Rooks show some-
what similar behaviour, but it is not found in the protectively coloured
partridge.

Many different means are adopted by birds for recognition of other
members of the species and of the same and opposite sex; bird-life

xvii. 4 MIGRATION 493

contains elaborate social and sexual rituals for many occasions. For
example, relief of the one bird by the other at the nest is accompanied
by a peculiar wing-flapping ceremony in herons and other birds.
Greeting ceremonies are common in many species, and there is a host
of sexual recognition and courtship rituals, to be considered later,
serving the immediate function of regulating the aggressiveness that
otherwise arises when two individuals approach each other closely.
Such ceremonies prevent attempted copulation with the same sex and
ensure it with a member of the opposite sex, and of the right species.
Apart from sexual behaviour birds show many complex mutual and
social reactions. Thus in communities of hens or pigeons there is
quickly established a rank of 'pecking order', such that each bird is
submissive to the one above it, the order changing, however, when age,
moulting, or experiment (e.g. sex-hormone injection) alters the state
of the birds. More pleasing communal habits are the dances and
corporate flights, which are well known in cranes and other species.

4. Bird migration and homing

Among the remarkable devices of birds is their habit of seasonal
movements to obtain the advantage of the favourable conditions
offered in more northerly regions only during the summer. The most
familiar migrations are those north and south (sometimes north-east
and south-west) over the land masses of the northern hemisphere, but
there are similar movements also in the southern hemisphere, though
they are of lesser extent. Some tropical birds migrate to breed in the
rainy season in the outer tropics, removing to the central tropics in
the dry season. Marine birds also may make extensive migrations.
Thus the great shearwater (Puffinus) breeds on Tristan da Cunha, but
comes as far north as Greenland or Iceland in May, returning again
after months of wandering at sea, apparently without making a land-
fall. The Arctic tern (Sterna) breeds in the north temperate zone, and
migrates to the Antarctic along both sides of the Atlantic. Penguins
make migrations by swimming. Distances up to 6,000 miles from
Northern Europe to South Africa have been recorded for swallows
and storks, and even farther for the Arctic tern. The factors deter-
mining the direction and course of migration are beginning to be
known. It has been shown that the power to follow a given course
depends partly on the ability to navigate by observation of the position
of the sun or stars (Matthews, 1955; Sauer, 1957). Birds certainly do
not learn the routes from their elders, indeed the young often leave
first. However, juveniles return only approximately to their birthplace,

BIRD BEHAVIOUR

494 lilKU bLHAVlUUK XVII. 4-

whereas older individuals return to their old nesting sites. Individual
memory therefore plays a part. The birds often migrate singly and

Fig. 302. Direction of migration of the stork (Ciconia). The black spots represent points

of recovery of birds ringed in Germany. The dotted areas show the pathways produced

by ecological and geographical factors. (After Schulz and Stresemann.)

experiments in a planetarium have shown that warblers turn accurately
in the appropriate direction as given by the stars.

The available evidence therefore suggests (a) that for most species
at least there is a preferred direction for migration, which is indepen-
dent of experience. Hand-reared warblers will orient correctly by the
stars without previous experience; (b) that they may be deviated by
features of the environment such as coastlines or hills; (c) that after

xvii. 5 MIGRATION 495

experience they can do more than just steer a course — they can navi-
gate, that is fix position, calculate the course to steer, and follow it.

Powers of 'homing' are remarkable in birds, altogether apart from
migration. It is probable that these feats are performed by the use of
visual clues, combined with a tendency to follow coastal outlines and
other conspicuous geographical features. Pigeons are trained to 'home'
by release at progressively increasing distances and can acquire the
ability to return from more than 500 miles.

It has now been satisfactorily proved that pigeons return home after
release from a distant point even if they have never been there before,
nor have had any previous training in returning from situations out of
sight from the loft. Matthews (1955) and others have shown that upon
release the birds fly off towards home provided that they can see the
sun. This capacity to navigate by the sun must depend upon deter-
mination of position on two coordinates by observations of the sun's
altitude, azimuth, and/or movement. This implies the use of a very
accurate chronometer as a means of determining the difference be-
tween home and local time. It is hard to believe that all this could be
achieved in the few seconds following release, but the facts demand
some such hypothesis. Moreover, experiments designed to upset the
'chronometer' by altering the period of daylight have been claimed to
be effective in altering the direction of flight of birds upon release.

Other birds are also able to return home from spectacular distances,
an instance being the Manx shearwater removed from its nest (burrow r )
on Skokholm Island off the Welsh coast and sent to Boston by air: it
returned in 12 days, the distance being 3,067 miles across the Atlantic.
In another experiment three out of ten untrained terns returned to
their nests from a distance of 855 miles, in about 6 days. There are
many peculiar and unexplained features about such long journeys.

5. The stimulus to migration

It is probable that the north-to-south migrations of birds in the
northern hemisphere take place under some stimulus provided by the
internal condition of the gonads, these being themselves affected by
the seasonal change. Rowan has made extensive experiments with
juncos, birds that are summer visitors to Alberta, Canada. If the birds
are caged in the autumn and illuminated to compensate for the shorten-
ing day the gonads do not regress as they normally do at that season,
so that full breeding song continues on into the middle of winter.
Rowan had the interesting idea of releasing these birds in the winter
and found that they immediately moved away, perhaps northwards,

496 BIRD BEHAVIOUR xvn. 5-

conditions being then appropriate if anything for that direction. On
the other hand, control birds, which had been kept in Alberta but
without extra light, showed no tendency to move away if released in
mid- winter. Since the gonads of these controls had, of course, by then
undergone reduction, the stimulus to migrate south was not felt. This
would agree with the fact that only some individuals of species such
as the thrush and blackbird migrate. These experiments suggest that
seasonal changes in illumination may be an important factor deter-
mining migration. However, they leave many points unsettled. For
instance, is there a stimulus that starts the bird migrating north again
if it has 'wintered' near the equator, where there is little or no seasonal
change ? It may be that once alteration of the gonads has been started,
say, by reduction in light, a cycle will be set up, the gonads developing
again with the longer days in the south and thus driving the bird north
again, and so on.

6. The breeding-habits of birds

The complexity and variety of bird behaviour show especially in
their breeding; perhaps in no other creatures except men is such
elaborate behaviour involved in bringing the birds together and caring
for the young. In order to ensure adequate provision for the develop-
ment of a warm-blooded animal and its nourishment until it can fend
for itself it is necessary either to keep it within the mother or to provide
a means of incubating the eggs. In either case a long period of care is
necessary after birth; the young animals, having a large surface area,
require a great amount of food to keep warm. Thus young starlings
and crows may eat as much as their own weight of food each day.

Mammals and birds set about providing for this warmth and food
in different ways. Since a female mammal can move about and get
food while pregnant the father can desert her altogether, though fre-
quently he does not do so. In birds the eggs and young cannot be left
cold for long and it is therefore especially desirable that the father
should help. In birds, therefore, perhaps even more than in mammals,
the breeding-habits involve the development of elaborate systems of
mutual relations, serving not only to bring the parents together but also
to keep them together throughout the period of incubation and while
feeding the young. The actual building of the nest may be an intricate
business in which both birds collaborate and a further factor is that
the pa